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ORIGIN AND EVOLUTION OF THE CARIBBEAN MANGROVES: PALYNOLOGICAL EVIDENCE Valentí Rull PDVSA Exploration and Production, Caracas, Venezuela. Postal address: PA 1394, PO box 025304, Miami-FL 33102-5304, USA. Email: rullv@pdvsa.com. Abstract Mangroves are forested ecosystems from tropical coasts that are dominated by a few tree genera resistant to the salinity of the seawater and with special morphological and physiological adaptations, which determine a characteristic physiognomy. The evolutionary origin of mangroves is commonly associated with the first appearances of fossil pollen and spores from elements of these communities and has been placed in the lower Cretaceous. In the present work, the available palynological evidence is analyzed, and an Eocene origin is proposed instead. The quantitative pollen analysis of a Paleocene/Eocene section from northern South America is examined as an example of a typical evolutionary sequence. The first mangrove elements appeared in the Paleocene, but the dominant and characteristic components did not appear until the lower Eocene. However, their relative abundance was too low to account for mangrove ecosystems. The first palynological records of well-established mangrove communities were found in the middle Eocene, where the more common elements occur and show characteristic abundances. The same trend has been observed in other localities from northern South America, suggesting that the first real mangrove communities in this region of Tethys appeared in the Eocene. The evolution of these mangroves has not been a gradual process. Stable phases have alternated with others of more intense speciation, expansions and reductions of the geographical range, and massive extinctions. An outstanding event in the evolution of mangroves took place in the Eocene/Oligocene boundary, coinciding with global mass extinctions, related with climatic changes. The main Eocene mangrove elements disappeared at that time and were replaced by other newly originated ones, from which the present mangroves derive. From the Oligocene onwards, a progressive taxonomic enrichment without remarkable extinctions has been the rule. Note. This paper is the English translation of a former paper published in Spanish approximately 20 years ago. The original reference is Rull, V. 2002. Origen y evolución de los manglares del Caribe: evidencias palinológicas. XIII Simposio de la Asociación de Palinólogos en Lengua Española (A.P.L.E.) (Cartagena, 27,28, 29 de Septiembre de 2000): libro de textos completos (Español), pp. 333-349. The translation has been performed by the author according to the original text, without any modification, correction or updating. Figures are original, and the text inside has not been translated. The present address of the author is Valentí Rull, Laboratory of Paleoecology, Geosciences Barcelona (CSIC), C. Llluís Solé i Sabarís s/n, 08028 Barcelona, Spain. Email: vrull@geo3bcn.cisc.es

mailto:rullv@pdvsa.commailto:vrull@geo3bcn.cisc.es

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Introduction Mangroves are among the most conspicuous and representative tropical ecosystems, covering most of the tropical coasts, in general, and those of the Caribbean coasts, in particular (Fig. 1). These forest communities grow in warm and wet climates or on coastal areas protected by sand bars or coral reefs and flooded by brackish to hypersaline waters. Mangroves develop a characteristic dark-green fringe on the distal part of the coasts, which contributes to stabilizing the coastal line by minimizing wave erosion and favoring sediment retention within the tangle of logs and aerial roots characteristic of mangrove trees. In the Caribbean, these mangrove trees are represented by Rhizophora spp. (red mangrove), Avicennia germinans (black mangrove) and Laguncularia racemosa (white mangrove). Locally, Pelliciera rhizophorae can also be an important component, but it is restricted to a small area of Central and South America (Winograd, 1983). These trees form dense, often monospecific, forest communities that constitute the structural basis for the development of ecotonal ecosystems where a high diversity of characteristic terrestrial and aquatic species thrive and interact.

Figure 1. Approximate distribution of mangroves (black bands) worldwide (a) and in the Caribbean region (b). Sampling localities mentioned in the text are highlighted by a triangle (outcrop) and a circle (well). CM = Maracaibo Basin. Base map from the World Conservation Monitoring Centre (http://www.wcmc.org.uk).

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The origin of mangroves and their biogeographical patterns is controversial. It is not unusual to confound the origin of mangroves with the origin of mangrove elements. Mangroves are communities, and their fossil record should not be restricted to a few appearances of some taxa supposedly of mangrove affinity. For example, the identification of Cordaites macrofossils with supporting aerial roots was once considered as evidence of a Carboniferous mangrove, but it was further demonstrated that this type of fossil was of continental origin (Plaziat, 1995). Similar situations occurred for Triassic, Jurassic and Cretaceous fossils (review in Tomlison, 1986; Plaziat, 1995). To properly document a mangrove community, it is necessary to find a characteristic and unequivocal mangrove taphocenose, which may be identified by comparison with sedimentary patterns from modern mangroves, by the occurrence of characteristic fossil associations, or both. Regarding the evolutionary process that has led to the extant biogeographical patterns of mangroves, Duke (1995) synthesized the existing hypotheses into two main groups, namely, the “dispersalists” and the “vicarianists”. According to the first group, the center of origin coincides with the center of diversity and, therefore, the main mangrove elements must have been originated in the Indo-Malay region (where taxonomic diversity is higher) and then dispersed to other continents. Contrastingly, the “vicarianists” assumed a more or less uniform Paleotropical origin of mangrove taxa and a further taxonomic differentiation in each continent favored by the formation of reproductive barriers as a result of continental drift. Most of these evolutionary hypotheses were based on the geographical distribution of extant taxa and implicitly assumed that mangrove evolution proceed as a continuum, that is, as a single gradual and uninterrupted trend. However, the fossil record of the Caribbean and adjacent areas does not support this view and favors the idea that paleogeographical and paleoclimatic shifts have determined the existence of at least two well-differentiated evolutionary steps, separated by the biological crisis of the Eocene/Oligocene transition. The Eocene Caribbean mangroves irreversibly disappeared, and the new mangroves developed from the Oligocene onwards, representing a large taxonomic and evolutionary lap, a resetting event from which a different evolutionary trend initiated, giving rise to modern mangroves. This paper aims to improve the knowledge of mangrove evolution in the Caribbean and adjacent regions by analyzing the available palynological evidence. The analysis focuses on two main points: the origin of mangroves as communities and the large evolutionary revolution that occurred in the Eocene/Oligocene transition, which was especially intense in the Caribbean region. The evolution of post-Eocene mangroves is still poorly documented in the Caribbean fossil record and will be developed on the basis of the available literature. Origin: the first palynological records The occurrence of mangroves in the tropical coasts since the Carboniferous has been a matter of speculation. However, supporting evidence has always been indirect and based mainly on the eventual association of fossils with marine sediments and unwarranted morphological speculations (Tomlinson, 1986; Plaziat, 1995). The first palynological records of mangrove elements correspond to the Upper Cretaceous and the Paleocene and include the fern Acrostichum aureum and the palm Nypa fruticans, as represented by the fossil sporomorphs Deltoidospora adriennis and Spinizonocolpites sp., respectively. Most of these records are from the Caribbean-Gulf of Mexico region and from other tropical areas of Africa, Asia and Oceania (Tanikaimoni, 1987; Graham, 1995). Other records proceed from regions of Europe and North America (Plaziat, 1995) that were situated in the tropical belt and connected to the former areas by the Tethys Sea during the Cretaceous and part of the Tertiary (Fig. 2).

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Figure 2. Positions of the main continental masses since the Late Cretaceous to the Miocene. The approximate correspondence with present-day continents is the following: NA – North America, SA – South America, EU – Europe, AS – Asia, AF – Africa, IN – India, AN –Antarctica, AU – Australia. Redrawn from Briggs (1987). Based on these findings, some authors propose the occurrence of Nypa-dominated mangroves since the Late Cretaceous, although they admit the lack of conclusive taphonomic evidence (Collinson, 2000). In the Caribbean area, the occurrence of mangroves during the Cretaceous and the Paleocene has been questioned for two main reasons. First, neither Acrostichum aureum nor Nypa fruticans are mangrove trees but accompanying species living on brackish waters behind the mangrove fringe, rather than on the distal part of the coasts (Tomlinson, 1986; Plaziat, 1995). These species lack the necessary physiological and morphological adaptations to constitute the structural basis of an ecosystem with the physiognomy and the specific features of mangroves. Second, most of the existing literature on the topic (review in Frederiksen, 1985; Tanikaimoni, 1987; Graham, 1995) uses qualitative (presence/absence) data, which are unsuitable to reconstruct past plant communities and, therefore, to record the occurrence of past mangrove ecosystems. Past community reconstructions should be based on quantitative palynological data, with statistically significant sample sizes, useful to reliably infer the taxonomic composition and the frequency distribution of each taxon. These fossil community reconstructions are usually performed by comparison with the abundance and distribution patterns of palynomorphs in present-day mangrove sediments (modern analogs). Unfortunately, this type of quantitative study is rare in pre-Quaternary sediments. An example of a quantitative study of this nature is from the Venezuelan Maracaibo Basin (Fig. 1) and consists of the statistical analysis of 147 samples from an outcrop (surface samples) and an exploratory well (core samples) extending from the Lower Paleocene to the Middle Eocene (Rull, 1998b, 1999, 2000). A large part of this sequence was used to establish the classical tropical palynological zonations (Germeraad et al., 1968; Muller et al., 1987), but, in spite of the

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existence of a great amount of statistically significant pollen analyses (Rull, 1987), the potential of these samples for quantitative reconstruction was not fully exploited. The sediments of this Paleocene-Eocene sequence were deposited on deltaic and shallow marine environments (Guasare, Marcelina and Misoa formations), as indicated by the lithological features and the presence of foraminifer taxa typical of such environments (González de Juana et al., 1980). Modern-analog studies (Rull, 1998c) and surveys developed in the upper Tertiary (Lorente, 1986) demonstrated that pollen from mangrove elements is abundant in deltaic and shallow-marine environments. However, in the studied sequence, mangrove pollen was scarce until the Middle Eocene (Fig. 3). During the Paleocene, the only important mangrove element was Deltoidospora adriennis (Acrostichum aureum), as part of a palynological assemblage representing the vegetation of brackish coastal swamps. Spinizonocolpites spp. (Nypa) was present in a single sample.

Figure 3. Abundance and composition of the different palynological associations since the Paleocene until the Middle Eocene, and vegetation types that they represent, according to Rull (1998b, 1999). Paleocene: P1 – Proxapertites operculatus, Retidiporites magdalenensis (unknown vegetation type); P2 – Ctenolophonidites lisamae, Echitriporites trianguliformis, Proxapertites sp., Proxapertites cursus (inland swamp forests); P3 – Psilatricolporites sp., Deltoidospora adriennis, Psilamonocolpites medius, Mauritiidites franciscoi (coastal swamps); Lower Eocene: EI1 – Striatricolpites catatumbus, Retitricolporites irregularis, Retibrevitricolpites triangulatus (inland swamp forests), EI2 – Retitricolpites amapaensis, Proxapertites operculatus (unknown vegetation type, similar to P1); EI3 – Verrucatosporites speciosus, Deltoidospora adriennis, Psilamonocolpites medius, Mauritiiditesfranciscoi (coastal swamps, similar to P3). Middle Eocene: EM1- Retitricolpites simplex, Retimonocolpites retifossulatus (alluvial plain forests); EM2- Retibrevitricolpites triangulatus, Mauritiidites franciscoi, Longapertites proxapertitoides (unknown vegetation type); EM3- Verrucatosporites speciosus, Psilamonocolpites medius, Retitricolpites amapaensis, Deltoidospora adriennis (coastal swamps, similar to P3); EM4 - Psilatricolporites crassus, Spinizonocolpites echinatus (Pelliciera mangroves).

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In the lower Eocene, the situation was similar – i.e., Acrostichum in the brackish-water association and Nypa scarce – but Pelliciera, represented by Psilatricolporites crassus, appeared in low amounts (

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species (Keller, 1986). Regarding the causes, the most accepted involve environmental changes, especially climatic changes. The most important factors for the removal of part of the Eocene biota, well-adapted to high temperature and moisture values, would have been an abrupt global cooling and a significant precipitation decrease that occurred during the Upper Eocene (Frakes, 1979; Rull, 1998a) (Fig. 4).

Figure 4. Synthetic oxygen isotopic curve obtained from marine cores from the Atlantic Ocean. Modified from Pickering (2000). Globally, the warmest Cenozoic phase included the Paleocene and the Eocene, which represented a continuation of the Cretaceous greenhouse world, when the Earth’s poles were ice-free, a situation that changed at the beginning of the icehouse world, in the Late Eocene/Oligicene (Pickering, 2000). These changes seem to have been related to the continental drift and the ensuing changes in the global oceanic and atmospheric circulation. Paleogeographic changes in the Tethys region seem to have been especially important for the occurrence of the global climatic cooling. In particular, the closure of the Tethys Sea interrupted the warm equatorial currents, and the progressive separation of continental masses favored the penetration of cold polar currents into the tropical zone. The separation of the Australian/South American from the Antarctic masses, which occurred during the Eocene, was especially significant in this respect (Fig. 2). In northern South America, the evolutionary change was marked by the appearance of a post-Eocene flora that already contained the major part of extant families and possibly genera (Muller, 1980). The mangrove flora was not an exception. Fig. 5 shows that the compositions of

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Eocene and post-Eocene mangroves were radically different due to the extinction of the main Eocene species and the evolutionary emergence of the post-Eocene ones (Rull, 1998a). During the Eocene, mangroves were dominated by the mangrove tree Pelliciera and the palm Nypa, whereas the fern Achrostichum occupied the most internal brackish water mangrove strip. Achrostichum is still living in the region without significant changes, but Nypa disappeared, and Peliiciera was drastically reduced in both abundance and geographical range. The extinction of Nypa was simultaneous in most tropical areas during the Eocene/Oligocene transition (Muller, 1980), but it still survives today in the SE Asian mangroves, where it is an important component (Tomlinson, 1986) (Fig. 6). The case of Nypa is not exceptional, as many angiosperm genera of pantropical distribution during the Eocene are presently restricted to SE Asia (Collinson, 2000). The occurrence of a global climate change seems insufficient to explain this general phenomenon. At present, Nypa lives in habitats with very warm and humid climates, with low precipitation seasonality. It has been proposed that an eventual seasonality intensification in the American and Euro-African tropics could have occurred during the Upper Eocene, causing the disappearance of Nypa from these areas (Germeraad et al., 1968; Muller, 1980).

Figure 5. Stratigraphic ranges of known mangrove genera (with indication of their approximate abundance) and other associated elements (presence/absence only) that occur in Caribbean mangroves (Graham, 1995; Rull, 1998a). Nypa is represented by the mangrove-tree genera because of its importance in the Eocene mangrove assemblages.

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However, another pantropical biogeographical factor could have been involved, as the disappearance of Nypa in the central and western Tethys regions coincided with the closure of the marine connection between them by the coalescence of Africa and Eurasia (Fig. 2), which could have affected the migration patterns. The continuity of coastal environments is essential for the existence of mangroves. For example, mangroves are absent today on Pacific islands between approximately 90°W (Galapagos Islands) and 170°W (Samoa), probably due to migration limitations due to the lack of continuity of coastal environments (Woodroffe & Gridrod, 1991; Duke, 1995). Environmental conditions seem not to be as limiting if we consider that human-introduced mangroves live normally in the Hawaiian Islands, situated in between (~155°W).

Figure 6. Geographical distribution of the most important mangrove taxa. A) Present distribution of Nypa and Pelliciera (solid lines) compared with their Eocene fossil records (dots). Raw data from Wijmstra (1968), Fuchs (1970), Pares et al. (1974), Winograd (1983), Jiménez (1984), Tomlinson (1986), Hoorn (1994), Graham (1995) and Rull (1998a). B) Distribution of extant Rhizophora species. Raw data from Muller & Caratini (1977) and Tomlinson (1986). The case of Pelliciera is similar but differs in two main aspects: (i) its fossil pollen has been found only in America, Africa and Europe (Thanikaimoni, 1987; Frederiksen, 1985), and (ii) its present geographical distribution is significantly smaller and geographically opposite to Nypa (Fig. 6). The progressive reduction of Pelliciera to its present geographical range has been explained by a gradual rainfall decrease, which would have relegated this mangrove tree to a few humid refugia (Jiménez, 1984). It has also been proposed that competition with other mangrove trees that evolved later could have displaced Pelliciera from its original range. The best candidate

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could have been Rhizophora (Graham, 1977), which has dominated Neotropical mangroves from the Oligocene to the present. The “new” mangroves: from the Oligocene to the present The first, albeit scarce, appearances of the present Rhizophora species, represented by the fossil pollen Zonocostites ramonae, were recorded at the end of the Eocene, when Nypa disappeared and Pelliciera began to decrease. The first post-Eocene mangroves were formed mainly by Rhizophora and Pelliciera, as other mangrove genera such as Avicennia, Laguncularia or Conocarpus were still absent (Fig. 5). By those times (Oligo-Miocene), the Tethys marine connection was already closed (Fig. 2), which determined the evolutionary isolation of the Neotropical, African and Asian mangroves. This would have led to the development of two different sets of Rhizophora species, one in the Neotropics and the Gulf of Guinea (R. mangle, R. racemosa, R. harrisonii) and another in SE Asia and eastern Africa (R. apiculata, R. mucronata, R. stylosa, R. lamarkii) (Fig. 6). The distribution of R. mangle is peculiar, as it also occurs in some Pacific islands at the east of Australia (New Caledonia, Fiji). The most characteristic and extended Caribbean species is R. mangle, which is adapted to a wide range of salinity, whereas R. racemosa is less tolerant to this parameter. R. harrisonii, which is a hybrid species of R. mangle and R. racemosa, has an intermediate tolerance to water salinity (Muller & Caratini, 1977). Owing to its importance in the formation of present mangrove communities worldwide and its early evolutionary origin, in comparison with the rest of post-Eocene mangrove elements, the genus Rhizophora could be fundamental for unraveling mangrove evolution. However, the evolution of Rhizophora is hard to follow through its fossil pollen record due to its scarcity and the difficulty of morphological differentiation among the pollen of the different Rhizophora species (Muller & Caratini, 1977; Thanikaimoni, 1987). Therefore, the origins of the biogeographical and ecological patterns of extant mangroves have been deduced primarily from speculations based on the present distribution of Rhizophora species, the changing position of continents over time and the personal preferences of researchers for a given general biogeographical theory (“dispersalism” or “vicarianism”). This has resulted in a set of different proposals that are still hard to verify with the available evidence. The dispersalists propose that mangroves diversified in their assumed Asiatic area of origin (Indo-Malaysia) and then migrated to other tropical zones, although a group believes that the dispersal occurred via the Pacific coasts (Van Steenis, 1962), whereas others propose that the dispersal took place across the Tethys coasts (Chapman, 1976). The defenders of the Pacific way argue that the Tethys coasts were too arid to sustain mangroves, whereas the others believe that the present absence of mangroves in the major part of the Pacific would be evidence of the unsuitability of the coasts of this ocean for mangrove development. The vicarianist point of view in mangrove evolution was introduced by McCoy & Heck (1976), who considered that the taxonomic diversification of these communities was the consequence of the fragmentation of their former pantropical distribution across the Tethys coasts. In the Caribbean region, the post-Eocene diversification was fundamental to attain the present mangrove composition. Considering both mangrove-tree species and their associated elements, the diversity increased from 7 genera in the Oligocene to 27 in the present, with no extinctions (Graham, 1995). Apart from Rhizophora, the most important mangrove genera have appeared gradually during the Miocene (Avicennia), the Pliocene (Laguncularia) and the Quaternary (Conocarpus). The emergence of new genera was generally slow until the Plio-Pleistocene, when it experienced a significant acceleration (Fig. 5). This coincided with the Late Cenozoic “Ice Age”, characterized by a significant intensification of the glacial-interglacial oscillations, characteristic of the icehouse world and the glaciaoeustatic cycles. Since the Late Pliocene, the relative sea-level oscillations increased drastically, not only in frequency (~100,000 years) but also in

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intensity (~100 m) (Vera, 1994). The lowest sea levels known to date were recorded during the Quaternary (Haq et al., 1988). All these environmental changes have led to substantial and periodic modifications of mangrove habitats as potential evolutionary drivers. References Briggs, J.C. 1987. Biogeography and Plate Tectonics. Elsevier, Amsterdam. Cavelier, C.; Chateauneuf, J.-J.; Pomerol, Ch.; Rabussier, D.; Renard, M. & Vergagnaud-Grazzini,

C. 1981. The geological events at the Eocene/Oligocene boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 36, 223-248.

Chapman, V.J. 1976. Mangrove Vegetation. J. Cramer, Vaduz. Collinson, M.E. 2000. Cenozoic evolution of modern plant communities and vegetation. In:

Culver, S.J. & Rawson, P.F. (eds.), Biotic Responses to Global Change. Cambridge University Press, Cambridge, pp. 223-243.

Duke, N.C. 1995. Genetic diversity, distributional barriers and rafting continents – more thoughts on the evolution of mangroves. Hydrobiologia 295, 167-181.

Frakes, L.A. 1979. Climates Throughout Geologic Time. Elsevier, Amsterdam. Frederiksen, N.O. 1985. Review of Early Tertiary sporomorph paleoecology. AASP Contributions

Series 19, 1-92. Fuchs, H.P. 1970. Ecological and palynological notes on Pelliciera rhizophoraceae. Acta Botancia

Neerlandica 19, 884-893. Germeraad, J.H.; Hopping, C.A. & Muller. J. 1968. Palynology of Tertiary sediments from tropical

areas. Review of Palaeobotany and Palynology 6, 189-348. Graham, A. 1977. New records of Pelliceria (Theaceae/Pelliceriaceae) in the Tertiary of the

Caribbean. Biotropica 9, 48-52. Graham, A. 1995. Diversification of Gulf/Caribbean mangrove communities through Cenozoic

time. Biotropica 27, 20-27. Haq, B.U., Handerbol, J. & Vail, P.R. 1988. Mesozoic and Cenozoic chronostratigraphy and

eustatic cycles. SEPM Special Publication 42, 71-108. Hoorn, C. 1994. Miocene Palynostratigraphy and Paleoenviromnents of Northwestern

Amazonia. Ph. D. dissertation, University of Amsterdam, The Netherlands. Jiménez, J.A. 1984. A hypothesis to explain the reduced ditribution of the mangrove Pelliciera

rhizophorae Tr. & Pl. Biotropica 16, 304-308. Keller, G. 1986. Stepwise mass extinctions and impact events: Late Eocene to Early Oligocene.

Marine Micropaleontology 10, 267-293. Lorente, M.A. 1986. Palynology and palynofacies of the upper Tertiary in Venezuela.

Dissertationes Botanicae 99. J. Cramer, Berlin. MacLeod, N.; Ortiz, N.; Pefferman, N.; Clyde, W; Schulter, C. & MacLean, J. 2000. Phenotypic

response of foraminifera to episodes of global envirorunental change. In: Culver, S.J. & Rawson, P.F. (eds.), Biotic Responses to Global Change. Cambridge University Press, Cambridge, pp. 51-78.

Meng, J. y McKenna, M. C. 1998. Faunal turnovers of Palaeogene mammals from the Mongolian Plateau. Nature 394, 364-367.

Molina, E. 1995. Modelos y causas de extinci6n masiva. Interciencia 20, 83-89. Muller, J. 1980. Palynological evidence of Paleogene climatic changes. Memoires du Museum

National d'Histoire Naturelle, Nouvelle Series, Series B Botanique XXVI, 211-218. Muller, J. 1981 . Fossil pollen records of extant Angiosperms. Botanical Review 47, 1-142. Muller, J. & Caratini, C. 1977. Pollen of Rhizophora (Rhizophoraceae) as a guide fossil. Pollen et

Spores XIX, 361-389. Pares, M., Uesugui, N. & Santos, A. 1974. Palinologia dos sedimentos Meso-Cenozoicos do Brasil.

Boletim Tecnico Petrobras 17, 177-191.

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Pickering, K.T. 2000. The Cenozoic world. In: Culver, S.J. & Rawson, P.F. (eds.), Biotic Responses to Global Change. Cambridge University Press, Cambridge, pp. 20-34.

Plaziat, J.-C. 1995. Modern and fossil mangroves and mangals: their climatic and biogeographic variability. Geological Society Special Publication 83, 73-96.

Prothero, D.R. & Berggren, WA. 1992. Eocene-Oligocene Climatic and Biotic Evolution. Princeton University Press, Princeton.

Rull, V. 1987. A note on pollen counting in palaeoecology. Pollen et Spores XXIX, 471-480. Rull, V. 1998a. Evoluci6n de los manglares neotropicales: la crisis del Eoceno. Interciencia 23,

355-362. Rull, V. 1998b. Middle Eocene mangroves and vegetation changes in the Maracaibo Basin,

Venezuela. Palaios 13, 287-296. Rull, V. 1998c. Modern and Quaternary palynological studies in the Caribbean and Atlantic

coasts of Northern South America: a paleoecologically-oriented review. Boletin de la Sociedad Venezolana de Geólogos 23, 5-24.

Rull, V. 1999. Palaeofloristic and palaeovegetational changes across the Paleocene/Eocene boundary in northern South America. Review of Palaeobotany and Palynology 107, 83-95.

Rull, V. 2000. Ecostratigraphic study of Paleocene and early Eocene palynological cyclicity in northern South America. Palaios 15, 14-24.

Rull, V, Vegas-Vilarrubia, T. & Espinoza, N. 1999. Palynological record of an early-mid Holocene mangrove in eastern Venezuela. Implications for sea-level rise and disturbance history. Journal of Coastal Research 15, 496-504.

Smith, G.A. ; Manchester, S.R., Ashwill, M., McIntosh, W.C. & Conrey, R.M. 1998. Late Eocene-early Oligocene tectonism, volcanism, and floristic change near Gray Butte, central Oregon. Geological Society of America Bulletin 110, 759-778.

Thanikaimoni, G. 1987. Mangrove palynology. Institute français de Pondichery, Travails de la Section Scientifique et technique 24, 1-100.

Tomlison, P.B. 1986. Mangrove botany. Cambridge University Press, Cambridge. Vera, J.A. 1994. Estratigrafia. Principios y Métodos. Ed. Rueda, Madrid. Westgate, J.W. & Gee, C.T. 1990. Palaeoecology of a middle Eocene mangrove biota

(vertebrates, plants and invertebrates) from southwest Texas. Palaeogeography, Palaeoclimatology, Palaeoecology 78, 163-177.

Wijmstra, T.A. 1968. The identity of Psilatricolporites and Pelliciera. Acta Botanica Neerlandica 17, 114-116.

Winograd, M. 1983. Observaciones sobre el hallazgo de Pelliciera rhizophorae (Theaceae) en el caribe colombiano. Biotropica 15, 297-298.

Woodroffe, C.D. & Grindrod, J. 1991. Mangrove biogeography: the role of Quaternary environmental and sea-level changes. Journal of Biogeography 18, 479-492.

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