Observaciones sobre Ceramium uruguayense (Ceramiaceae, Rhodophyta): primer registro para el Mar Caribe

María A. Solé¹

¹ Estación de Investigaciones Marinas de Margarita. Fundación La Salle de Ciencias Naturales. Apartado 144, Porlamar 6301. Isla de Margarita, Venezuela. *Autor para correspondencia:msole@edimar.org

Recibido: 27 de agosto de 2007.
Aceptado: 13 de julio de 2008.

ABSTRACT

The red algae Ceramium uruguayense is reported for the first time in the Caribbean Sea. The vegetative and reproductive morphology of this species are described. Ceramium uruguayense is compared with other similar Caribbean species. Ceramium uruguayense has clear diagnostic characters like 8–9 periaxial cell, presence of pseudoperiaxial cells, acropetal direction in nodal formation and basipetal growth from periaxial cell. A distribution analysis of the genus in the Caribbean is presented.

Key words: Ceramium uruguayense, Rhodophyta, Caribbean, morphology.

RESUMEN

El alga roja Ceramium uruguayense es reportada por primera vez para el Mar Caribe. Se describe la morfología vegetativa y reproductiva de esta especie. Ceramium uruguayense es comparada con otras especies similares presentes en el Caribe. Ceramium uruguayense tiene caracteres diagnósticos claros como son 8–9 células periaxiales, presencia de células pseudoperiaxiales y formación del nudo con dirección acropétala así como crecimiento basipétalo desde la célula periaxial. Se presenta un análisis de la distribución geográfica del género para la región del Caribe.

Palabras clave: Ceramium uruguayense, Rhodophyta, Caribe, morfología.

INTRODUCTION

In Venezuela, the genus Ceramium is represented by 13 species: Ceramium brasiliense Joly (Ganesan, 1989), C. brevizonatum var. caraibicum H. E. Petersen et Børgesen (García & Vera, 2004), C. cimbricum H. E. Petersen in Rosenvinge (Ganesan, 1989), C. comptum Børgesen (Gómez, 1998), C. dawsonii A. B. Joly (Ganesan, 1989), C. deslongchampsii Chauvin ex Duby (Ganesan, 1989), C. diaphanum (Lightfoot) Roth (Ganesan, 1989), C. floridanum J. Agardh (Ganesan, 1989), C. luetzelburgii O. C. Schmidt (García & Gómez, 2005a), C. nitens (C. Agardh) J. Agardh (Ganesan, 1989), C. tenerrimum (G. Martens) Okamura (Gómez, 1998), C. vagans P. C. Silva (García & Gómez 2005b), and the currently reported C. uruguayense Taylor (Taylor, 1960).

Ceramium species are often difficult to identify since they are somewhat variable in morphology and some species have been inaccurately described.

During a review of the Evangelina marine algal collection of M. Díaz–Piferrer in the Herbarium MOBR, a specimen of Ceramium uruguayense from the north coast of the Margarita Island (Nueva Esparta State, Venezuela) was found and confirmed by comparison with the holotype.

MATERIALS AND METHODS

Specimens of Ceramium uruguayense were studied from the Evangelina collection deposited in the Herbarium MOBR of the Margarita Station of Marine Investigations from Fundación La Salle de Ciencias Naturales. Specimens were either pressed or preserved in 4% formalin sea water. The measurements of the nodes were made between fifth and sixth dichotomies starting from the apex. For the observation of axial and periaxial cells, cross section of the thallus was made through the upper part of the axial cell in the middle part of plant. The cortical band and cortication was studied based on the taxonomic criteria for the genus following Dixon (1960), Womersley (1978) and South and Skelton (2000). Acropetal and basipetal cortical cells measurements were made on the first cells near the periaxial cells. Microscope slide preparations were stained with 0.1% safranine and mounted in 15% fenolized corn syrup. Measurements were made using a Manostat vernier and micrometer for microscope to provide the (lowest), average, and (highest) measurement for the feature and the standard deviation is given in parentheses (SD). Abbreviations/symbols: : female gametophyte, : male gametophyte, : tetrasporophyte, v: vegetative. For distribution analysis of the genus in the Caribbean, a revision of the literature in the region was done.

RESULTS

Ceramium uruguayense W. R. Taylor (1960: 532 – 533, Pl. 65: Figs. 3, 4)

Vegetative morphoanatomy: Plants are erect, epiphytic, 5 cm in height and are attached by uniseriate unicellular and multicellular rhizoids that originate from periaxial cells only at the base of plant. The rhizoids are up to 287 µm long. The principal branching pattern is alternate in one plane and subdichotomous in the secondary branches which occurs every 5–6 nodes along the main axis. Adventitious branchlets of unlimited growth are present. The apices are slightly incurved. The branch tips may be convergent or divergent and up to 0.45 mm long and (94.3) 164.47 (266.5) (SD: 9.36) µm in diameter.

The axial cells are hyaline and in surface view (237.8) 253.79 (282.9) (SD: 13.45) µm wide x (262.4) 283.72 (303.4) (SD: 13.08) µm long. In the middle portion of the plant, the nodes are (254.2) 397.69 (550.8) (SD: 46.31) µm in diameter. The internodal distance measures (45.1) 131.6 (324) (SD: 71.1) µm. In the upper part of the plant, the cells are shorter bringing the nodes very close together. Cortication occurs only at the nodes. The cortical node length is (73.8)184.2 (237.8) (SD: 42.82) µm. The periaxial cells that develop the cortication are oval and number 8 to 9 per node. They occur in rows and are (12.3) 28.07 (41) (SD: 6.9) µm wide x (16.4) 40.61(57.4) (SD: 7.32) µm long in transversal cut.

Pseudoperiaxial cells are produced laterally from the periaxial cells in number eight to nine per node, (16.4) 21.67 (28.7) (SD: 3.9) µm wide x (36.9) 38.7 (41) (SD: 2) µm long. These pseudoperiaxial cells sometimes can divide to form one smaller pseudoperiaxial basipetal cell. The cortical bands consist of approximately five–six cell rows originating by the aggregation of four conspicuous corticated filaments. Each periaxial cell giving rise to four cells in two directions, two acropetally and two basipetally. The first acropetal cells are formed by dichotomic divisions of the first acropetal cells, so acropetal filaments are four to eight cells long, with four acropetal rows. Final divisions of acropetal filaments could be not dichotomic, just in one direction. Basipetal filaments are formed by dichotomic divisions of the first basipetal cells and are two to four cells long with two basipetal rows.

Reproductive morphoanatomy: Tetrasporangia emergent, tetrahedrical, pigmented and produced in whorls in the cortical bands. They are developing from the periaxial cells, are only on the branches of limited growth and (32.8) 78.38 (184.5) (SD: 59.1) µm in diameter. They are partially covered by cortical cells. Each fertile node is enlarged and contains one to four tetrasporangia.

Carpogonial branches develop at the apices of principal and secondary branches at the top of the plant. Gonymocarps are produced from the first periaxial cell and are three celled as described for the genus. The gonymocarp's cells are smaller than the trichogyne and are smaller when compared with the proximal cortical cell. The gonymocarps occurs 2–3 together on the abaxial side of the secondary branches and are surrounded by 5–6 sterile involucral branchlets, are spherical and terminal, and also projected above the surface of the branches. They appear to originate from periaxial cells. The gonymocarps are globulate and (61.5) 153.89 (243) (SD: 58.63) µm in diameter and (90.2) 157.1 (274.7) (SD: 93.86) in length. The carpospores are pyramidal, granulated in appearance, and (20.5) 29.11 (32.8) (SD: 4.08) µm long.

Spermatangia are globose, hyaline, and (4.1) 5.13 (6.15) (SD: 1.45) µm in diameter and (8.2) 9.6 (12.3) (SD: 2.37) µm in length. They develop from the cortical cells superficially and are dispersed over the nodes at young lateral branchlets and cover their nodes and the internodal zones but do not have defined borders.

Habitat: Commonly grows epiphytic on species of the genus Corallina L, Bryothamnion Kützing, Grateloupia C. Agardh, Codium Stackhouse and Ulva L.

material examined: Uruguay: Holotype, puerto La Paloma, 6 December 1925, Schmitt 277, MICH 17895 (). These numbers are from MOBR, Venezuela: Margarita Island, Juangriego Beach, 12 Mach 1966, M. Díaz–Piferrer E–9714 (v); 12 March 1966, M. Díaz–Piferrer E–2041 (–); 12 March 1966, M. Díaz–Piferrer E–1798 (–);Tolete Point, 23 April 1966, M. Díaz–Piferrer E–1800 (,);Tacuantar Point, 23 April 1966, M. Díaz–Piferrer E–1799 (); El Paujil, La Guardia, 24 April 1966, M. Díaz–Piferrer E–1801 (v); Tacuantar Point, 8 June 1966, M. Díaz–Piferrer E–1802 (,).

Aditional examined material: Ceramium brasiliense, numbers are from MOBR. Brazil: Saco de Ribeira Beach, Baía de Flamingo, Ubatuba, Estado de Sao Paulo, 16 November 1963, M. Díaz–Piferrer E–9639 (v); Parana Beach, Municipio de San Vicente, Estado de Sao Paulo, 29 November 1963, Díaz–Piferrer & A. Joly E–1684 (––); Saco de Ribeira Beach, Baía de Flamingo, Ubatuba, Estado de Sao Paulo, 29 November 1963, M. Díaz–Piferrer E–9812 (v).

DISCUSSION

Comparative morphology. Ceramium uruguayense is described for the first time from the Caribbean. Based on morphoa–natomical features, the Venezuelan specimens coincide with the taxonomic circumscription of the holotype specimen (table 1). Ceramium uruguayense was described by Taylor (1960) based in specimens from Punta del Este, Uruguay collected by Schmitt in 1925. In the diagnosis of C. brasiliense Taylor (op. cit.) commented that this plant could represent a "depauperate form of C. uruguayense".

Ceramium uruguayense has similitude with another Caribbean species like C. brasiliense, C. floridanum J. Agardh, C. filicula Harvey ex Womersley and C. brevizonatum var. caraibicum Petersen et Børgesen. The principal diagnostic character to separate Ceramium uruguayense and C. brasiliense is the presence of pseu–doperiaxial cells; these are not present in C. brasiliense and the number of periaxial cells which are eight to nine in C. uruguayense and six in C. brasiliense (Barreto & Yoneshigue–Valentin, 2001; Barros–Barreto et al., 2006). These aspects have been found to be valid diagnostic features for separating these species so the taxo–nomic status of both species in the western Atlantic is confirmed.

Ceramium floridanum is a little knows species, clear nodal cortication studies haven't been carried out to this species. C. floridanum is similar to C. uruguayense because is alternately branched and erect, but in contrast has nodes with cortication composed of 1–3 transversal series of cells, which extend equally up and down to the internodal zone and no pseudoperiaxial cell have been recorded for it (Taylor, 1960; Ríos,1972; Schneider & Searles, 1991).

Ceramium brevizonatum var. caraibicum is characterized by the presence pseudoperiaxial cells and eight to nine periaxial cells like C. uruguayense but differs from this, in the cortication with just one to two acropetal rows (Barros & Yoneshigue–Valentin, 2001; García & Vera, 2004; Barros–Barreto et al., 2006) in contrast with three to four acropetal rows and two basipetal rows in C. uruguayense.

Ceramium uruguayense differs from C. filicula (Barros–Barreto et al., 2006) in the presence of eight to nine periaxial cells, the presence of pseudoperiaxial cell and three to four acropetal rows.

Ceramium geographical distribution. Table 2 shows distribution of the Ceramium species in the Caribbean. More than 85% of the western Atlantic species are distributed in the Caribbean from the northern limit of the Yucatan Peninsula, Mexico, to the western coast of Venezuela. The main incidence per region occurs in the northern Caribbean with 18 species of Ceramium, 14 of which are reported for Cuba (Suárez, 2005). Also the genus has a good representation in the southern region specifically in Colombia, Lesser Antilles and Venezuela. The species with the in the Caribbean region is C. nitens in the entire Caribbean region (except in Trinidad and Tobago). C. uruguayense is restricted to the south western tropical Atlantic and C. brasiliense is reported in the Caribbean only for Cuba (Suárez, 2005) and Venezuela (Lemus, 1984).

Ceramium uruguayense is previously thought to be endemic to Uruguay in the subtropical western Atlantic. This temperate specie is now known that is present in the western region of Margarita Island, Venezuela. This species is not uncommon along this Venezuelan coastal area. Upwelling and cooler nutrient rich waters coincide with its occurrence.

Díaz–Piferrer (1967) has noted the effect of this upwelling on the marine flora along the western coast of Venezuela and is more intense over the continental shelf of the north coast of Margarita Island (Juangriego Beach, Tacuantar Point) where surface temperatures of 19–23°C give rise to a temperate zone enclave within which the benthic marine flora is markedly affected and where the temperate species of algae are commonly present during the first part of the year.

ACKNOWLEDGMENTS

The author is grateful for the loan of the holotype from the MICH Herbarium. Thanks to Paola Pardo for the help in the lab process. Thanks to Joaquín Buitrago, Yocie Yoneshigue, Mutue Toyota, Abel Sentíes, Krem Osle and two anonymous reviewers for improving this paper with their critical reading. Contribution No. 371 from Margarita Station of Marine Investigations (Edimar), Fundación La Salle de Ciencias Naturales

REFERENCES

Ballantine, D. 1990. Ceramium bisporum (Rhodophyta, Ceramiales) an unusual new species from deep–water habitats in the Caribbean. Phycologia 29: 146–149.        [ Links ]

Ballantine, D. & N. Aponte. 2002. A checklist of the benthic marine algae known to Puerto Rico. Second revision. Constancea 83. University and Jepson. Herbaria, P.C. Silva Festschrift. http://ucjeps.berkeley.edu/constancea/83/ballantine_aponte/check–list.html.        [ Links ]

Barreto, M. B. B. & Y. Yoneshigue–Valentin. 2001. Aspectos morfológicos do gênero Ceramium Roth (Ceramiaceae, Rhodophyta) no estado do Rio de Janeiro. Hoehnea 28: 77–110.        [ Links ]

Barros–Barreto, M., L. McIvor, C. A. Maggs And P. C. Gomes. 2006. Molecular systematics of Ceramium and Centroceras (Ceramiaceae, Rhodophyta) from Brazil. Journal of Phycology 42: 905–921.        [ Links ]

Bula–Meyer, G. 1986. Las macroalgas de los arrecifes coralinos de las Islas del Rosario, costa Caribe de Colombia. Boletín Ecotropica 14: 3–20.        [ Links ]

Bula–Meyer, G. & R. schnetter. 1988. Las macroalgas recolectadas durante la Expedición Uraba II, costa Caribe del noreste Chocoano, Colombia. Boletín Ecotropica 18: 19–32.        [ Links ]

Castellanos, P. , R. Varela & F. Muller–Karger. 2002. Descripción de las áreas de surgencia al sur del Mar Caribe examinadas por el sensor infrarrojo AVHRR. Memoria de la Fundación La Salle de Ciencias Naturales 154: 55–76.        [ Links ]

Collado, L., I. Ortegón, A. Sentíes, L. Comba & J. González. 1998. Macroalgae of Puerto Morelos Reef System, Mexican Caribbean. Hidrobiológica 8: 133–143.        [ Links ]

Díaz, M., E. Torres & J. Espinoza. 1998. Lista de algas del área de protección Yum Balam, Quintana Roo, México. Revista de Biología Tropical 46: 487–492.        [ Links ]

Díaz–Piferrer, M. 1967. Efectos de las aguas de afloramiento en la flora marina de Venezuela. Caribbean Journal of Science 7: 1–13.        [ Links ]

Díaz–Piferrer, M. 1968. Ceramiella jolyi a new species of rhodophyta from Puerto Rico. Caribbean Journal of Science 8: 199–205.        [ Links ]

Díaz–Piferrer, M. 1970. Adiciones a la flora marina de Venezuela. Caribbean Journal of Science 10: 159–193.        [ Links ]

Díaz–Pulido, G. & M. Díaz–Ruiz. 2003. Diversity of benthic marine algae of the Colombian Atlantic. Biota Colombiana 4: 203–246.        [ Links ]

Dixon, P. 1960. Studies on marine algae of the British Isles: the genus Ceramium. Journal of the Marine Biological Association of the United Kingdom 39: 331–374.        [ Links ]

Duncan, E. & L. Lee. 2006. A checklist of the marine macroalgae of the Republic of Trinidad and Tobago. Caribbean Marine Studies 7: 1–95.        [ Links ]

Ganesan, E. 1989. A Catalog of Benthic Marine Algae and Seagrasses of Venezuela. Conicit, Fondo Editorial, Caracas. 237 p.        [ Links ]

García, M. & B. Vera. 2004. Ceramium brevizonatum var. caraibicum H. E. Peterson & Børgesen (Ceramiaceae, Rhodophyta) nuevo registro para la costa venezolana. In: Resúmenes del Primer Congreso Sudamericano de Ficología, 7, Lima. Universidad Nacional Agraria La Molina, Perú.        [ Links ]

García, M. & S. Gómez. 2005a. Ceramium luetzelburgii O. C. Schmidt nuevo registro de Ceramiaceae para la costa venezolana. In: Resúmenes, XVI Congreso Venezolano de Botánica, Monagas. Universidad de Oriente, Monagas, Venezuela.        [ Links ]

García, M. & S. Gómez. 2005b. Ceramium vagans P. C. Silva (Ceramiaceae, Rhodophyta), nuevo record de la ficoflora de Venezuela. In: Resúmenes, LV Convención Nacional Asovac, Caracas. Universidad Central de Venezuela, Venezuela.        [ Links ]

Ginés, H., C. L. Angell, M. Méndez, G. Rodríguez, G. Febres, R. Gómez, J. Rubio, G. Pastor & J. Otaola. 1972. Carta Pesquera de Venezuela 1. Areas del Nororiente y Guayana. Fundación La Salle de Ciencias Naturales. Monografía 16. Caracas. 328 p.        [ Links ]

Gómez, S. 1998. Rhodophyta (algas marinas rojas) del Parque Nacional Archipiélago Los Roques. Tesis Doctoral. Facultad de Ciencias. Universidad Central de Venezuela. Caracas. 299 p.        [ Links ]

Joly, A. B. 1957. Contribuição ao conhecimento da flora ficológica marinha da baía de Santos e alrededores. Universidade de São Paulo, Faculdade de Filosofía, Ciencias e Letras, Botanica 14 (217): 7–196.        [ Links ]

Kapraun, D. F. 1972. Notes on the benthic marine algae of San Andrés, Colombia. Caribbean Journal of Science 12: 199–203.        [ Links ]

Lemus, A. 1984. Las algas marinas del Golfo de Paria, Venezuela. II. Rhodophyta. Boletín del Instituto Oceanográfico de Venezuela 23: 55–112.        [ Links ]

Littler, D. S. & M. M. Littler. 1997. An illustrated marine flora of the Pelican Cays, Belize. Bulletin of the Biological Society of Washington 9: 1–149.        [ Links ]

Littler, D. S. & M. M. Littler. 2000. Caribbean Reef Plants. Offshore Graphics Inc., Washington, D.C. 542 p.        [ Links ]

Ríos, N. 1972. Contribución al estudio sistemático de las algas macroscópicas de las costas de Venezuela. Acta Botanica Venezuelica 7: 219–324.        [ Links ]

Schneider, C. W. & R. B. Searles. 1991. Seaweeds of the southeastern United States. Cape Hatteras to Cape Canaveral. Durham & London, Duke University Press. 553 p.        [ Links ]

Schnetter, R. 1980. Algas marinas nuevas para los litorales colombianos del mar Caribe. Caribbean Journal of Science 15: 121–125.        [ Links ]

Soto, R. & D. Ballantine. 1986. La flora bentónica marina del Caribe de Costa Rica (Notas preliminares). Brenesia 25/26: 123–162.        [ Links ]

South, G. & P. Skelton. 2000. A review of Ceramium (Rhodophyceae, Ceramiales) from Fiji and Samoa, South Pacific. Micronesica 33: 45–98.        [ Links ]

Suárez, A. 2005. Lista de las macroalgas marinas cubanas. Revista de Investigaciones Marinas 26: 93–148.        [ Links ]

Taylor, W. R. 1960. Marine Algae of the Eastern Tropical and Subtropical Coasts of the Americas. The University of Michigan Press. Ann Arbor, Michigan. 870 p.        [ Links ]

Womersley, H. B. S. 1978. Southern Australian species of Ceramium Roth (Rhodophyta). Australian Journal of Marine & Freshwater Research 29: 205–257.        [ Links ] ]]> 1990 29 146-149 2002 83 2001 28 77-110 2006 42 905-921 1986 14 3-20 1988 18 19-32 2002 154 55-76 1998 8 133-143 1998 46 487-492 1967 7 1-13 1968 8 199-205 1970 10 159-193 2003 4 203-246 1960 39 331-374 2006 7 1-95 1989 237 2004 2005 2005 1972 16 328 1998 299 1957 14 217 217 7-196 1972 12 199-203 1984 23 55-112 1997 9 1-149 2000 542 1972 7 219-324 1991 553 1980 15 121-125 1986 25/26 123-162 2000 33 45-98 2005 26 93-148 1960 870 1978 29 205-257