Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

Beatriz Barreto, María; Barreto, Eduardo First report of Rhizophora racemosa meyer (Rhizophoraceae) in the mangrove forests of the venezuelan caribbean coast Interciencia, vol. 37, núm. 2, febrero, 2012, pp. 133-137 Asociación Interciencia Caracas, Venezuela

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María Beatriz Barreto and Eduardo Barreto-Pittol

SUMMARY

Rhizophora racemosa G.F.W. Meyer is reported for the first diagnostic character used to distinguish the species is the or- time in mangrove forests of the Venezuelan Caribbean Coast. der of the number of bifurcations in the inflorescence. Descrip- The specimens were collected in the Cariaco River and the tion of the habitat of this species is included. Gulf of Santa Fe, on the western coast of Sucre State. The

Primer reporte de Rhizophora racemosa Meyer (Rhizophoraceae) en los manglares de la costa Caribe de Venezuela María Beatriz Barreto y Eduardo Barreto-Pittol RESUMEN Se reporta por primera vez la presencia de la especie Rhi- estado Sucre. El carácter diagnóstico empleado para diferen- zophora racemosa G.F.W. Meyer en los manglares de la costa ciar la especie fue el orden en el número de bifurcaciones de Caribe de Venezuela. Los ejemplares fueron recolectados en el la inflorescencia. También se mencionan algunas observaciones río Cariaco y el golfo de Santa Fe, en la costa occidental del del hábitat de R. racemosa.

PrimeIrO reLATÓRIO de Rhizophora racemosa Meyer (Rhizophoraceae) Nos manguEs da costa DO Caribe dA Venezuela Maria Beatriz Barreto e Eduardo Barreto-Pittol RESUMO Relata-se por primeira vez a presença da espécie Rhizo- Sucre. O carácter diagnóstico empregado para diferenciar a phora racemosa G.F.W. Meyer nos mangues da costa do Ca- espécie foi a ordem no número de bifurcações da inflorescên- ribe da Venezuela. Os exemplares foram recolhidos no rio cia. Também se mencionam algumas observações do hábitat Cariaco e no golfo de Santa Fe, na costa ocidental do estado de R. racemosa.

Introduction able salinity. They are gener- ecosystems (Duke et al., In the ACEP region, three ally restricted to areas where 1998). Ten Rhizophora taxa species of the genus Rhi- Mangroves are intertidal the average air temperature have been recognized world- zophora have been recog- ecosystems present in tropical during the coldest months wide in two bio-geographical nized: R. mangle (L.), R. and subtropical coastlines, exceeds 20°C and the sea- regions: the Indo-West-Pacific harrisonii Leechman and exposed to variable hydrologi- sonal variation in temperature (IWP) and the Atlantic-Carib- Leechman, and R. racemosa cal conditions as a result of does not exceed 10°C (Walsh, bean-Eastern-Pacific (ACEP; G.F.W. Meyer (Leechman, tidal flushing and freshwater 1974; Chapman, 1977; Tom- Duke, 1992; Duke et al., 2002; 1918; Salvoza, 1936; Keay, sources, and characterized by linson, 1994). Nettel and Dodd, 2007). The 1953; Prance et al., 1975; Ji- being hypoxic or anoxic, hav- The genus Rhizophora is the latter includes the tropical and ménez, 1987). Some authors ing organic and mineral sub- most common of the three subtropical coasts of America, indicate that R. harrisonii is strates, textures ranging from genera found in woodland the Caribbean islands and a hybrid of the other two clay-like to sandy, and vari- habitats that dominate these western Africa (Figure 1). species (Breteler, 1969; Tom-

KEYWORDS / Cariaco River / Caribbean Coast of Venezuela / Gulf of Santa Fe / Rhizophora racemosa / Salinity / Received: 09/29/2011. Modified: 01/31/2012. Accepted: 02/01/2012.

María Beatriz Barreto. Ph.D. in y Ecología Tropical, UCV. Ad- e-mail: maria.barreto@ciens. Eduardo Barreto. B.S. in Geo- Ecology, Universidad Central dress: Universidad Central de ucv.ve chemistry, UCV, Venezuela. de Venezuela (UCV). Research Venezuela. P.O. Box 47058. Scientist, Instituto de Zoología Caracas 1041-A. Venezuela.

FEB 2012, VOL. 37 Nº 2 0378-1844/12/02/133-05 $ 3.00/0 133 linson, 1994; Dodd et al., grove strip, 65m from the 1995). Cerón-Souza et al. lagoon’s edge, west of the (2010) maintain that R. Nurucual River and east of harrisonii possibly repre- the Santa Fe River. sents a morphotype result- 3- The flood zone in the ing from the backcrossing village of Santa Fe and introgressive hybrid- (10°16’46”N, 64°25’46”W), ization between R. mangle which is fed by a nameless and R. racemosa. drainage running more or R. mangle, which has a less parallel to the Santa wider distribution, is Fe River 1.3km to the east. spread throughout the wet- Here a relict mangrove of lands and dry coasts of what was possibly a wet- America. The other two land located in the Santa species, R. racemosa and Fe River flood plain, be- R. harrisonii, are restricted fore entering the Gulf of to more humid climates in Figure 1. Distribution of the taxa Rhizophora throughout the Atlantic-Caribbean- Eastern-Pacific (ACEP) biogeographical region. Santa Fe, was observed. areas that have lower sa- linity and regular fresh TABLE I water flows (Afzal-Rafii et al., LATITUDINAL BOUNDARIES FOR THE DISTRIBUTION OF THE THREE SPECIES 1999; Duke et al., 2002; Duke OF THE GENUS Rhizophora IN AMERICA and Allen, 2006; Figure 1; Atlantic Ocean Pacific Ocean Table I). R. racemosa is Species found on the Pacific coast of North South North South America, from Puerto Lobos, Rhizophora mangle L. Bermuda (32º20') Praia do Sonho, Puerto Lobos, Tumbes River, Mexico, to Punta Malpelo, Brazil (27º53') Mexico (30º15') Peru (3º40') Tumbes River, Peru. On the eastern coast of America it is R. harrisonii Leechman Yaguaraparo River, Preguiças River, Chantuto, Guayas River, distributed from Yaguaraparo, Venezuela (10º30') Brazil (2º40') Mexico, 15º 15' Ecuador (2º30') Gulf of Paria, Venezuela, to R. racemosa G.F.W. Meyer Yaguaraparo River, Maranhense Gulf, Lempa River, Guayas River, Maranhense Gulf, Brazil, and Venezuela (10º30') Brazil (2°45') El Salvador (13º17') Ecuador (2º20') in the Caroní River estuary located on the western coast Sources: Salvoza (1936), Jiménez (1985), Santos (1986), Lacerda et al. (2001). of Trinidad (Bacon, 1993). R. mangle, the dominating er and the Gulf of Santa Fe 1- The mangrove forests bor- At each site, samples of taxon in the mangroves of reported here represents a dering the whole length of the interstitial water were col- Venezuela, has been reported new finding for the Venezue- Cariaco River, all the way to lected at a depth of 20cm throughout continental and lan Caribbean coast and its estuary in the Gulf of Ca- around the trunks of trees insular coasts that have dry to broadens the distribution of riaco (10°29'42''-10°29'34''N, identified as R. racemosa, and humid climates. The distribu- the species in the ACEP re- 63°38'33''-63°37'55''W), in salinity was measured with a tion of R. racemosa, however, gion. the external part of the man- refractometer calibrated for had been confined to the es- grove strip, in the low inter- seawater (Atago). Units are tuaries of the drainage basins Sampling Areas tidal zone. expressed in parts per thou- of the Atlantic in Venezuela, sand (ppth). 2- Near the road that runs par- including the Orinoco River R. racemosa specimens We examined the exsiccatae allel to the La Bodega Lagoon Delta, the San Juan River and were collected in (Figure 2): deposited as Rhizophora at (10°16'43''N, 64°23'59''W), in the coastal mud plains of the the National Herbarium of the internal part of the man- Gulf of Paria (Breteler, Venezuela (VEN) and the 1969; MARNR, 1986; Isidro Rafael Bermúdez Ro- Medina and Francisco, dríguez Herbarium (IRBR) 1997; Vegas-Vilarrúbia (Cumaná, Universidad de Ori- and López, 2008). ente), the available literature, In his revision of the and several on-line databases Atlantic species of Rhi- regarding this genus. No pre- zophora, Breteler (1969) vious record of R. racemosa recognized among the was found for the Venezuelan samples collected in Ven- Caribbean coast, the Carib- ezuela specimens of R. bean basin or the Gulf of racemosa in Yaguaraparo, Mexico. Paria Peninsula, Sucre State; the San Juan and Results and Discussion Guarapiche rivers, Mona- gas State; and Pedernales, The genus Rhizophora, Delta Amacuro State. Figure 2. Sites on the Cariaco River and in the Gulf of Santa Fe where the ob- present in woodland habitats, The presence of R. rac- servations were made and the specimens collected. The distribution of R. race- is characterized by having emosa in the Cariaco Riv- mosa along the Venezuelan Atlantic coast is shown. aerial prop roots, opposite,

134 FEB 2012, VOL. 37 Nº 2 TABLE II INFLORESCENCE CHARACTERISTICS USED TO DISTINGUISH THE Rhizophora SPECIES (ADAPTED FROM CERÓN-SOUZA et al., 2010). Order of the number Number of Species of bifurcations in flowers the inflorescence R. mangle 1, 2 2, 3, 4, 5 R. harrisonii 3, 4, 5 8, 16, 32 R. racemosa 5, 6, 7 32, 64, 128

counted in situ was 47 to 100 of Rhizophora form mixed (Figure 3). stands with trees growing 25- The trunks of the speci- 35m high. Environmental mens observed in the Cariaco conditions allow the three River varied in diameter from species to coexist in mixed 10 to 30cm and the height of stands with a high degree of the trees varied from 7 to structural development (Bre- 15m. The average interstitial teler, 1969; Medina et al., salinity of the samples col- 2008). Breteler adds that eco- lected at a depth of 20cm logical separation is possible was 2.3ppth. only where salinity conditions Sewage water from the vil- are extreme. lages surrounding the Santa The restricted distribution Fe flood plains and the La of R. racemosa along the Bodega Lagoon drain directly more humid areas of the Pa- into the mangroves. At this cific coast from El Salvador Figure 3. Rhizophora racemosa Meyer. Inflorescence of a specimen site R. racemosa grows in to Ecuador and along South collected in the mangrove forests of the Gulf of Santa Fe. The order of monospecific patches near R. America’s eastern coast from the bifurcations is indicated. mangle stands. R. racemosa Brazil to Venezuela (Gulf of trees measured on average Santa Fe) can be explained by simple, whole, deciduous character chosen was the 11m (8-14m) in height and 10- the reduction of its range dur- leaves, each pair associated number of sequential bifurca- 36cm in stem diameter. The ing the Miocene-Pliocene, and with a pair of lanceolate stip- tions in the inflorescence. The soils are more clayey than more recently during the last ules that leave an annular number of bifurcations (b) in those of the Cariaco River, glacial period. During the scar. The inflorescences are R. racemosa varies from 5 to and the average interstitial Plio-Pleistocene glaciations, axillary with perfect flowers. 7, and the number of flowers salinity at a depth of 20cm variations in sea levels pro- The seeds start to germinate (n) is related to the number of was 20ppth. duced significant changes in even when the fruit is still bifurcations (n= 2b; Table II). Savory (1953) studied the the extension of mangrove attached to the plant; hence Prance et al. (1975), in their ecology of the genus Rhi- forests: when sea levels were the propagules have extended description of the three spe- zophora in Nigeria and found high, distribution expanded; hypocotyls (Salvoza, 1936). cies of Rhizophora in the that when the three taxa oc- when they were low, it con- These viviparous plants are Neotropics, also consider bi- cur in sympatry, R. racemosa tracted (Van der Hammen, dispersed by water to great furcation in the inflorescence grows upstream bordering the 1974). It is possible that R. distances, and they can re- as a diagnostic character. The tributaries in very wet soils. racemosa had a wider range main viable for over one year authors indicate that the inflo- The distribution and spatial of distribution in the ACEP (Rabinowitz, 1978). rescence is axillary, in a di- segregation of the three spe- region and that changes in The morphological charac- chotomous panicle, with 5 to cies of Rhizophora have been climate (drops in temperature teristics used to distinguish 6 successive bifurcations in R. attributed to a differential tol- and humidity) and sea levels the three species of Rhizopho- racemosa and 3 to 5 in R. erance to salinity (Jonker, during the Late Quaternary ra are ramification; number of harrisonii. 1959; Savory, 1953). Ukpong reduced its population, caused flowers and length of inflores- The number of sequential (2000) found that in Nigerian local extinctions and ultimate- cence; peduncle length; form bifurcations in the inflores- mangroves growing in habi- ly led to a reduced range of and type of flower bud apex; cence was the diagnostic tats with varying physio- distribution along the Ameri- and length of the hypocotyl character used to determine graphical aspects, such as to- can Caribbean coast (Jiménez, (Keay, 1953; Hou, 1960; Bre- the species in the samples pography and morphometry, 1984). Climate conditions dur- teler, 1969; Jiménez, 1987). examined in the present R. racemosa was the dominat- ing the Quaternary glaciation In a study on hybridization study, both those deposited in ing species in topographically limited colonization or led to and introgression of the genus the herbariums and those col- lower areas, always bordering extinction, and, consequently, Rhizophora in the Neotropics, lected in the Gulf of Santa Fe the tributary canals, a fact the to the specie’s reduced distri- Cerón-Souza et al. (2010) dis- and the Cariaco River, which author ascribed to a higher bution range in the Caribbean tinguish the species based on had inflorescences with 6 to 9 tolerance to flooding. and the Gulf of Mexico. Duke the characteristics of the in- bifurcations. The number of In the San Juan River in et al. (1998) point out that the florescence. The diagnostic flowers per inflorescence Venezuela, the three species absence of R. racemosa along

FEB 2012, VOL. 37 Nº 2 135 the Central American Atlantic racemosa, its establishment in the Atlantic coast of Central manistic Development of the coast can be explained by the Gulf of Cariaco and its America (Nettel and Dodd, Universidad Central de Vene- extinction processes that took later expansion and dispersal 2007). The restricted gene zuela for financing the project place when conditions were to the Gulf of Santa Fe. flow in the Caribbean region Preliminary biological and unfavorable for the species. The last connection of the provides evidence that hydro- environmental characteriza- After a long period of con- Gulf of Cariaco to the Carib- logical factors, such as cur- tion of the Chacopata, Bo- traction in their range of dis- bean Sea was ~11,500 years rents (intensity and direction), caripo, Campoma and Buena tribution, mangroves have ex- ago (Van Daele et al., 2011). and terrestrial factors, such as Vista Lagoons in the Araya panded along coastal areas In the present, only a few riv- the existence of insular or Peninsula, Sucre State, Vene- since the last ice age (Duke et ers and streams drain directly continental barriers, configu- zuela, Nº 03-00-6654-2007, al., 1998; Saenger, 1998; into the Gulf of Cariaco. Of ration of the continental shelf, and Ernesto Medina for con- Dodd et al., 2002). The drain- these, the Cariaco River, coastal geomorphology or cli- structive comments on an ear- age and outflow of rivers in which drains into the gulf’s mate, may be restricting the lier draft. more humid areas may have eastern extremity, is the larg- range of distribution of R. created refuges for man- est and has the most signifi- racemosa throughout the Ca- REFERENCES groves. The species that sur- cant output. During part of ribbean region. vived in these refuge areas the Quaternary, the Man- Research into the genetic Afzal-Rafii Z, Dodd RS, Fauvel may have dispersed to sur- zanares and Casanay rivers, variability of R. racemosa, MT (1999) A case of natural selection in Atlantic-East-Pa- rounding regions via step-by- two important rivers with with the purpose of assessing cific Rhizophora. Hydrobiolo- step colonization once favor- relatively large drainage ba- if colonization or re-coloniza- gia 413: 1-9. able conditions returned. sins and significant sediment tion processes originated in Bacon PR (1993) Mangroves in the Long-distance dispersal loads, flowed into the Gulf of the populations located along Lesser Antilles, Jamaica and (LDD) seems to have played Cariaco. the Atlantic coast, and deter- Trinidad and Tobago. In Lac- an important part in the spo- It could also be proposed mining the direction of colo- erda LD (Ed.) Conservation and Sustainable Utilization of radic colonization events in that populations of R. race- nization on the South Ameri- Mangrove Forests in Latin the recent history of Rhi- mosa in the Gulf of Santa Fe can Atlantic coast, will allow America and Africa Regions. zophora in the Neotropics acted as areas of refuge, and to answer some of the ques- Part I. Latin America Man- (Cerón-Souza et al., 2010). dispersed by LDD to the Gulf tions regarding the diversifica- grove Ecosystems Technical Evidence of LDD has also of Cariaco at the end of the tion and dispersal of R. race- Reports Vol. 2. ITTO/ISME Project PD114/90. pp. 155-210. been obtained for A. germi- Quaternary, once the Carib- mosa, and to establish if ex- nans (Nettel and Dodd, 2007) bean Sea was reconnected to tinction processes can account Breteler FJ (1969) The Atlantic species of Rhizophora. Acta and the mangrove-associated the Gulf. This colonization, for the current disjunction in Bot. Neerl. 18: 434-444. species Hibiscus pernambu- however, may have occurred parts of the Caribbean region Chapman VJ (1977) Introduction. censis (Takayama et al., more recently due to the step- and the western Atlantic. In Chapman VJ (Ed.) Wet 2006). by-step process of LDD from Coastal Ecosystems: Ecosys- Two possible pathways can the Atlantic coasts of southern Material Examined tems of the World. Elsevier. be postulated for the recent Venezuela (Orinoco River), New York, USA. pp. 1-29. dispersal and colonization of Guyana, Surinam and Brazil VENEZUELA: Delta Ama- Cerón-Souza I, Rivera-Ocasio E, R. racemosa throughout Ven- to the Gulf of Paria, Trinidad Medina E, Jiménez JA, Mc- curo State: Manamo Creek, Millan WO, Bermingham E ezuela’s eastern Caribbean and the gulfs of Cariaco and Orinoco River, 01/31/1964 (2010) Hybridization and intro- coast. First, through an an- Santa Fe, as a result of the (9°55'N, 62°15’'W), F. Breteler gression in New World red cient channel connecting the North Brazil Current, which 3555 (VEN); Araguabisí mangroves, Rhizophora (Rhi- gulfs of Paria and Cariaco, carries masses of water with Creek, 10/15/1977 (9°10'N, zophoraceae). Am. J. Bot. 97: and, second, by migration and sediments from the Orinoco 61°06'W), J. Steyermark 945-957. dispersal along the northern and Amazon rivers into the 114660 (VEN); Monagas Chérubin LM, Richardson PL (2007) Caribbean current vari- coast of the Paria and Araya Caribbean Sea (Chérubin and State: Colorado Creek, San ability and the influence of the Peninsulas. Richardson, 2007). In the Juan River, 05/8/1966, F. Bre- Amazon and Orinoco freshwa- Macsotay (2005) has pro- northern part of the Gulf of teler 5152 (VEN); Francés ter plumes. Deep-Sea Res. 54: posed a so-called Humboldt Paria 7000-year old man- Creek, San Juan River, 1451-1473. channel, a shallow marine groves have been documented 05/9/1966, F. Breteler 5162 Dodd RS, Fromard F, Rafii ZA, corridor connecting the gulfs at 9.2m beneath the current (VEN); San Juan River, Blasco F (1995) Biodiversity among West African Rhi- of Paria and Cariaco, dating sea level. These are the oldest 05/10/1966, F. Breteler 5169 zophora: Foliar wax chemis- from the Early Pleistocene Quaternary mangroves regis- (VEN); San Juan River, try. Biochem. Syst. Ecol. 23: (1.8-1.54Ma), running 240km tered in Venezuela (Rull and 05/9/1966, F. Breteler 5163 859-868. from east to west, and fed by Vegas-Vilarrúbia, 1999; Ve- (VEN); Francés Creek, San Dodd RS, Afzal-Rafii Z, Kashani masses of water influenced by gas-Vilarrúbia and Rull, Juan River, 05/22/1967, J. N, Budrick J (2002) Land bar- the currents of the Guyanas. 2002). Wessels 1802 (VEN); San riers and open oceans: effects on gene diversity and popula- However, the two gulfs may In the ACEP region, in ad- Juan River, 05/9/1966, F. Bre- tion structure in Avicennia have been connected more dition to the Central Ameri- teler 5163 (VEN); Sucre State: germinans L. (Avicenniaceae). recently, ~120,000 years, ago can Isthmus (CAI) that acts San Juan River, w/o date, M. Mol. Ecol. 11: 1327-1338. when the sea level was higher as a land barrier, there is evi- Sanabria, w/o number (IRBR). Duke NC (1992) Mangrove floris- than it is today (Van Daele et dence, based on the cpDNA tics and biogeography. In Rob- al., 2011). This connection of A. germinans, of a restrict- ACKNOWLEDGEMENTS ertson AI, Alongi DM (Eds.) between the gulfs of Paria ed gene flow from the west- Tropical Mangrove Ecosys- tems. American Geophysical and Cariaco may have al- ern Atlantic coast to the Ca- The authors thank the Union. Washington, DC, USA. lowed for the dispersal of R. ribbean region and throughout Council for Scientific and Hu- pp. 63-100.

136 FEB 2012, VOL. 37 Nº 2 Duke NC, Allen JA (2006) Rhi- Keay RW (1953) Rhizophora in mangrove recolonization and drifted seeds. Mol. Ecol. 15: zophora mangle, R. samoensis, West Africa. Kew Bull. 8: dispersal along tropical coasts. 2871-2881. R. racemosa, R. × harrisonii 121-127. Evolution 61: 958-971. Tomlinson PB (1994) The Botany (Atlantic-East Pacific red man- Lacerda LD, Conde JE, Kjerfve B, Prance GT, Silva MFD, Albuquer- of Mangroves. Cambridge Uni- groves), version 2.1. In Elev- Álvarez-León R, Polanía J que BW, Araújo IJD, Carreira versity Press. New York, NY, itch [(Ed.) Species Profiles for (2001) American mangroves: lMM, Braga MMN, Macedo USA. 423 pp. Pacific Island Agroforestry. In Lacerda LD (Ed.) Mangrove M, Conceição PN Da, Lisbôa Ukpong IE (2000) Gradient analy- Permanent Agriculture Re- Ecosystems. Function and PLB, Braga PL, Lisbôa RCL, sources (PAR). Holualoa, HI, sis in mangrove swamp for- Management. Springer. New Vilhena RCQ (1975) Revisão ests. Trop. Ecol. 41: 25-32. USA. www.traditionaltree.org York, USA. pp. 1-62. taxonômica das espécies ama- Van Daele M, van Welden A, Mo- Duke NC, Ball MC, Ellison JC Leechman A (1918) The genus zônicas de Rhizophoraceae. (1998) Factors influencing bio- Acta Amaz. 5: 5-22. ernaut J, Beck Ch, Audemard Rhizophora in British Guiana. F, Sánchez J, Jouanne F, Car- diversity and distributional Kew Bull. 1: 4-8. Rabinowitz D (1978) Dispersal gradients in mangroves. Global rillo E, Malavé G, Lemus A, Macsotay O (2005) The Humboldt properties of mangrove propa- De Batist M (2011) Recon- Ecol. Biogeogr. Lett. 7: 27-47. gules. Biotropica 10: 47-57. Channel: Early Pleistocene struction of Late-Quaternary Duke NC, Lo EYY, Sun M (2002) extensional graben through Rull V, Vegas-Vilarrúbia T (1999) sea- and lake-level changes in Global distribution and ge- eastern Venezuela and Trini- Surface palynology of a small a tectonically active marginal netic discontinuities of man- dad. Caribb. J. Earth Sci. 39: coastal basin from Venezuela basin using seismic stratigra- grove emerging patterns in 83-91. and potential paleoecological phy: The Gulf of Cariaco, NE the evolution of Rhizophora. applications. Micropaleontolo- MARNR (1986) Conservación y Venezuela. Mar. Geol. 279: Trees 16: 65-79. gy 45: 365-393. Manejo de los Manglares 37-51. Hou D (1960) A review of the ge- Costeros en Venezuela y Trini- Saenger P (1998) Mangrove vege- Van der Hammen T (1974) The nus Rhizophora. Blumea 10: dad-Tobago. Serie de Informes tation: an evolutionary pers- Pleistocene changes of vegeta- 625-634. Técnicos DGIIA/IT/259. Min- pective. Mar. Freshw. Res. 49: tion and climate in tropical Jiménez JA (1984) A hypothesis to isterio del Ambiente y los Re- 277-286. South America. J. Biogeogr. 1: explain the reduced distribu- cursos Naturales Renovables. Santos M (1986) Considerações 3-26. tion of the mangrove Pelliciera Caracas, Venezuela. 123 pp. sobre a ocorrência de Rhizo- Vegas-Vilarrúbia T, Rull V (2002) rhizophorae Tr. & Pl. Biotro- Medina E, Francisco M (1997) phora harrisonii Leechman e Natural and human distur- pica 16: 304-308. Osmolality and 13C of leaf tis- Rhizophora racemosa G.F.W. bance history of the Playa Me- Jiménez JA (1985) Rhizophora sue of mangrove species from Meyer, no litoral do estado do dina mangrove community mangle L. Red Mangrove. environments of contrasting Maranhão, Brasil. Bol. Lab. (Eastern Venezuela). Caribb. J. SO-ITF-SM-2. US Forest Ser- rainfall and salinity. Estuar. Hidrobiol. São Luis, Mara- Sci. 1-2: 66-76. nhão 7: 71-91. vice. Silvics Manual. Institute Coast. Shelf Sci. 45: 337-344. Vegas-Vilarrúbia T, López P (2008) of Tropical Forestry. Puerto Medina E, Francisco M, Quilice A Salvoza FM (1936) Rhizophora. Nat. Edaphic patterns as related to Rico. 7 pp. (2008) Isotopic signatures and Appl. Sci. Bull. 5: 179-237. β-diversity in swamp forests Jiménez JA (1987) A clarification nutrient relations of plants in- Savory HJ (1953) A note of the and meadows of the Lower on the existence of Rhizophora habiting brackish wetlands in ecology of Rhizophora in Ni- Orinoco Delta plain (Venezu- species along the Pacific coast the northeastern coastal plain geria. Kew Bull. 1: 127-128. ela). Wetlands 28: 616-631. of Central America. Brenesia of Venezuela. Wetlands Ecol. Takayama K, Kajita T, Murata J, Walsh GE (1974) Mangroves: a re- 28: 25-32. Manag. 16: 51-64. Tateishi Y (2006) Phylogeogra- view. In Reimhold RJ, Queen Jonker FP (1959) The genus Rhi- Nettel A, Dodd RS (2007) Drifting phy and genetic structure of WH (Eds.) Ecology of halo- zophora in Suriname. Acta propagules and receding Hibiscus tiliaceus: Speciation phytes. Academic Press, New Bot. Neerl. 8: 58-60. swamps: Genetic footprints of of a pantropical plant with sea- York, NY, USA. pp. 51-174.

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