Botanica Marina 54 (2011): by Walter de Gruyter Berlin Boston. DOI /BOT

Transcription

1 Botanica Marina 54 (2011): by Walter de Gruyter Berlin Boston. DOI /BOT Notes on marine algae in the International Biosphere Reserve Seaflower, Caribbean Colombian I: new records of macroalgal epiphytes on the seagrass Thalassia testudinum Margarita Rosa Albis-Salas 1,2 and Brigitte Gavio1,2, * 1 Universidad Nacional de Colombia, Sede Caribe, Circunvalar San Luis Free Town # 52-44, San Andr é s Isla, Colombia 2 Departamento de Biología, Universidad Nacional de Colombia, Sede Bogot á, Ciudad Universitaria, Bogot á, Colombia, bgavio@unal.edu.co * Corresponding author Abstract Six species of macroalgae are newly reported for the Caribbean International Biosphere Reserve Seafl ower. All the algae were found growing epiphytically on Thalassia testudinum in shallow ( < 1 m) meadows around San Andr é s Island. Two of these species, Stylonema alsidii and Colaconema hypneae, have been previously reported from Colombian waters, whereas Chroodactylon ornatum, Colaconema dasyae, Colaconema hallandicum and parca are new records for Colombia. Keywords: Colombia; epiphyte; ; marine algae; new records. Introduction The marine benthic flora of Caribbean Colombia is relatively well known. The first phycological collections date back to 1832 for the Santa Marta region and and 1857 around Cartagena (Bula -Meyer 1998 ). In 1938, Schmitt collected several algae from the island of Old Providence (Taylor 1939 ). The following year, Taylor, on the Allan Hancock Expedition in the Caribbean, also sampled in Colombian waters. All these collecting efforts were summarized by Taylor (1960), who listed 109 species from Colombia, without specifying the sites of collection. Reinhardt Schnetter studied the marine flora of Colombia, focusing efforts on the area of Santa Marta and Islas del Rosario (Cartagena). His work was published in two books, Marine algae of the Caribbean coast of Colombia I: Phaeophyceae (Schnetter 1976 ) and Marine algae of the Caribbean coast of Colombia II: Chlorophyceae (Schnetter 1978 ). Starting in the 1980s, Bula-Meyer worked on the marine macroalgae of Colombia, and, like Schnetter, centered his attention on the Santa Marta region and the National Natural Park Tayrona. In 1998, he synthesized all knowledge on the Colombian marine flora, reporting a total of 472 species for the Caribbean coast of the country (Bula -Meyer 1998 ). Barriga -Bonilla et al. (1969) published a list of marine algae from the Archipelago of San Andr é s, Old Providence and Saint Cataline, in which 18 species were reported for San Andr é s Island; later, Kapraun (1972) reported 47 species for the island including those reported by Barriga -Bonilla et al. (1969). In his two books, Schnetter (1976, 1978) listed 62 species for San Andr é s and 39 species for Old Providence and Saint Cataline, but these lists did not include red algae. D í az-pulido and Bula-Meyer (1997) published the most complete report for the Archipelago, reporting 171 taxa for the oceanic keys (excluding the main islands). The Archipelago was declared an International Biosphere Reserve by UNESCO in 2001 because of the diversity and conservation status of its marine ecosystems. With a marine area of almost 350,000 km 2, it is the eighth largest marine reserve in the world. However, this reserve remains one of the least studied regions of Colombia. Díaz-Pulido and Díaz-Ruíz (2003) reported a total of 201 species for the entire Archipelago in the latest Colombian macroalgal checklist. Considering the marine area of the Archipelago, and the few published macroalgal studies, it is clear that the marine benthic flora has been greatly overlooked. In particular, there are no studies on the taxonomic composition of the epiphytic flora of Thalassia beds in Colombia. Recent field surveys of macroalgal epiphytes on Thalassia leaves in San Andr é s Island revealed species previously unknown to the region. Six new records of red macroalgae for the Archipelago, four of which are also new records for Colombia are presented here. Materials and methods Study environment San Andrés ( N; E) is situated in the southwestern Caribbean (Figure 1 ). It is part of the Archipelago of San Andr é s, Old Providence and Saint Cataline with an emergent area of approximately 25 km 2 (IGAC 1986 ). The island lies in the transition zone between tropical dry and tropical wet climates with trade winds mitigating the dry and warm climates. The annual mean temperature is 27.4 C, with a maximum between 29 C and 30 C (May June) and minimum between 25.5 C and 26.0 C (December February). The annual mean precipitation is mm; rain is unevenly distributed between the dry season (January April), with stronger winds, and a wet season (October December) when 80 % of the annual rain falls. During the period of May July

2 538 M.R. Albis-Salas and B. Gavio: New algal records in Caribbean Colombia as epiphytes on the encrusting algae Hydrolithon farinosum (J.V. Lamouroux) D. Penrose et Y.M. Chamberlain and Pneophyllum fragile K ü tzing, which covered up to 80 % of the Thalassia testudinum leaf surfaces. Many of the epiphytes were fertile, and some included tetrasporophytic, carposporophytic, and gametophytic phases (e.g., parca ). New records for both the Archipelago and Colombia are marked with an asterisk (*) below. Rhodophyta Order Stylonematales Family Stylonemataceae * Chroodactylon ornatum (C. Agardh) Basson Figure 1 San Andrés Island (Caribbean Colombia) showing study sites. Punta Hansa ( N; W), Harbor ( N; W), Bahía Hooker ( N; W), Bahía Honda ( N; W), La Mansión ( N; W), and Rocky Cay ( N; W). the rains are moderate (IDEAM 1995 ). The island harbors 400 ha of seagrass beds ( D í az et al ) dominated by Thalassia testudinum Banks et Sol. ex K.D. Koenig. Field and laboratory studies During the wet (December 2007) and dry seasons (March 2008) we sampled in six sites, on the east coast of the island (Figure 1) (for site descriptions, see Gavio et al ). All meadows were shallow ( < 1 m). The leaves of Thalassia were preserved in a 4 % formalin/seawater solution. Epiphytic algae were removed from leaves, stained with a 1 % aniline-blue solution (1 g aniline blue in 100 ml distilled water), mounted on slides in 50 % glycerin, and observed using an Olympus (Tokyo, Japan) BX 51 microscope. Information on the type localities of these taxa was obtained from Silva s Index Nominum Algarum ( ). Results and discussion Six new algal records for San Andr é s Island are reported here, of which four are also new records for Colombia. The algae were all diminutive filamentous Rhodophyta growing mostly Type locality Lake Mälaren, near Stockholm, Sweden. Uniseriate filaments to 800 µ m tall, subdichotomously branched, attached by means of a basal cell (5 6 µm diameter). Cells are squared, ovoid to elongate, 4 6 µ m in diameter and 5 13 µ m long, forming irregular rows in a gelatinous matrix, up to 10 µ m thick (Figure 2 ); blue-green to pale green. Site and season of collection Wet season 7 10 December, 2007, Bah í a Honda, Bah í a Hooker, Harbor, Punta Hansa, Rocky Cay; dry season March, 2008, Bah í a Honda, Harbor, La Mansi ó n, Punta Hansa, Rocky Cay. Known Caribbean distribution Bahamas, Cuba, Florida, Hispaniola, Texas, Venezuela, Virgin Islands. Remarks This species was never observed growing directly attached to Thalassia testudinum leaves, but was always epiphytic on Hydrolithon farinosum, Pneophyllum fragile, Polysiphonia spp., Chondria spp., and other red algae that were epiphytic on T. testudinum. Chroodactylon ornatum was described as sparingly branched by Schneider and Searles (1991). However, the San Andr é s specimens were observed to be both sparingly (Figure 2) branched and others profusely branched. Stylonema alsidii (Zanardini) K.M. Drew Type locality Trieste, Adriatic Sea. Thallus filamentous, unbranched to 1 mm high, dark red, mostly uniseriate with multiple cell rows irregularly arranged below (Figure 3), attached to the host by means of a basal cell, 8 µ m diameter, 9 µ m long. Cell divisions are intercalary with cells quadrate, cylindrical, elongate, globose, subglobose, flattened or irregular, 7.5 µm diameter, µ m long. The cells are embedded in a transparent, gelatinous matrix to 5 µm thick. Site and season of collection Wet season 31 March, 2008, La Mansi ó n; dry season 30 March, 2008, Harbor. Known Caribbean distribution Bahamas, Barbados, Belize, Brasil, Colombia, Cuba, Florida, Jamaica, Martinique, Texas, Tobago, Venezuela, Virgin Islands. Remarks The morphological difference between Chroodactylon ornatum and Stylonema alsidii is based upon the

3 M.R. Albis-Salas and B. Gavio: New algal records in Caribbean Colombia 539 Figures Chroodactylon ornatum. Habit. Scale bar = 50 µm. 3. Stylonema alsidii. Filament with multiple cell rows. Scale bar = 20 µm. 4. Colaconema hypneae. Erect filaments arising from cells of the prostrate system. Scale bar = 20 µm. 5. Solitary monosporangia in series. Scale bar = 20 µm. 6. Colaconema dasyae. Solitary monosporangia in series. Scale bar = 20 µm. 7. Colaconema hallandicum. Habit and basal cell. Scale bar = 50 µm. branching pattern (sparingly branched for C. ornatum vs. abundantly branched for S. alsidii ) (Schneider and Searles 1991 ). However, this character was found to be highly variable and not reliable. The two species were distinguished based chiefly on the color of the thallus, deep red in S. alsidii and greenish blue in C. ornatum, as suggested by Dr. M. Wynne (personal communication). Order Colaconematales Family Colaconemataceae Colaconema hypneae (B ø rgesen) A.A. Santos et C.W.N. Moura Type locality Eastern bay in harbor of St. Thomas, US Virgin Islands. Thallus filamentous, delicate, to 900 µ m in height; branching unilateral to irregular, sparse proximally, abundant distally. The alga has a prostrate filament system that sometimes coalesces into a multicellullar, pseudoparenchymatous disc. The erect filaments may arise from each cell of the prostrate system or the basal disc (Figure 4). Cells cylindrical, µm diameter, ( 100) µ m long; the basal cells are longer than the rest. Each cell contains one lobate plastid. Apical cells are 8 10 µm diameter, µ m long. Monosporangia ovoid, single, lateral, solitary or in series on one-celled stalks, µm diameter, µ m long (Figure 5). Site and season of collection Wet season 9 December, 2007, Bahía Hooker. Known Caribbean distribution Virgin Islands. Colombia, Florida, Texas, Remarks The San Andrés specimens fit the description of Colaconema hypneae for its spreading filamentous prostrate system (Figure 4), the size of most cells, and solitary or in series monosporangia (Figure 5). However, tapering apical cells as

4 540 M.R. Albis-Salas and B. Gavio: New algal records in Caribbean Colombia described by Schneider and Searles (1991) and B ø rgesen (1915) were not observed. Furthermore, these previous authors stated that cells in this species reach no more than 30 µ m in length, but cells up to 100 µ m were occasionally observed in the San Andr é s specimens. Schneider and Searles (1991) do not mention the presence of basal rhizoids originating from the basal disc. Børgesen (1915) described Acrochaetium seriatum for a specimen with endophytic filaments originating from the basal disc; however, in his discussion he mentioned that this new taxon was very similar to Acrochaetium hypneae (now C. hypneae ), and its only distinguishing feature was the endophytic filaments. At present, A. seriatum is considered a synonym of C. hypneae. * Colaconema dasyae (Collins) Stegenga, I. Mol, Prud homme van Reine et Lokhorst Type locality Woods Hole, MA, USA. Plants are caespitose, filaments uniseriate, arising from a panduriform basal cell, µ m. This cell forms, with two other lateral cells, the basal portion of the alga. Erect filaments are irregularly to unilaterally branched, sparse below, abundant above; cells are cylindrical, µm diameter, µm long. Monosporangia borne singly, ovoid, with one-celled stalk, 8 10 µm diameter, µ m long (Figure 6). Site and season of collection Dry season 30 March, 2008, Punta Hansa. Known Caribbean distribution Costa Rica, Lesser Antilles. *Colaconema hallandicum (Kylin) Alfonso-Carillo, Sanson, Sangil et Diaz-Villa Type locality Coast of Halland, Sweden. Thallus filamentous, pink, delicate, to 800 µ m high, arising from an ovoid spore, 8 10 µ m diameter, producing one or two erect filaments, irregularly to alternately branched, tapering towards the apices (Figure 7). Branchlets arise from the distal end of the cell at a 45 angle. Cells cylindrical, µm diameter and µ m long, each containing a single lobate parietal plastid which occupies the whole cytoplasm. Monosporangia single, lateral with one-celled pedicels, ovoid, 10 µ m diameter and 20 µm long. Site and season of collection Wet season 8 11 December, 2007, Bah í a Honda, Bah í a Hooker, Harbor, La Mansi ó n, Punta Hansa and Rocky Cay; dry season 30 March, 2008, Harbor and Punta Hansa. Known Caribbean distribution Venezuela, Virgin Islands. Order Ceramiales Family Rhodomelaceae * parca Setchell Cuba, Hispaniola, Florida, Type locality Arue Reef, Tahiti, South Pacific. Thallus filamentous, µ m high, formed by a prostrate axis from which upright branches arise. The upright branches are arranged in a precise pattern, with three determinate branches followed by an indeterminate branch without naked nodes between branches (Figures 8 and 9). Prostrate axis ecorticate, µ m diameter, cell wall µ m thick, segments 1 2 diameters long, with eight pericentral cells per segment, apices curved upward. Erect axes not branched, strongly arched when young, with truncated apices, slightly tapering towards the base, with 7 10 spiraled segments, µm diameter, diameters long. Each branchlet has 2 3 trichoblasts, which are four times alternately, unilaterally or pseudodichotomously ramified. The chloroplasts have a distinctive disc shape and appear as stacks in the cell. Unicellular rhizoids µ m diameter and µ m long, terminating in simple or digitate attachment pads. Rhizoids are cut off from pericentral cells and arise distally on the segment and may develop opposite or lateral to the erect filaments arising from the same segment. Tetrasporangia are formed on fertile determinate branches in 4 7 successive segments, but with the proximal 4 7 and distal 2 3 segments remaining sterile (Figure 10). Tetrasporangia spherical, µ m diameter, tetrahedrally divided, and arranged in spiral or straight series. Spermatangial stichidia oblong, 1 2 per branch, up to 65 µm diameter and 250 µ m long (stalk included in the measurement), terminal on branchlets. The stichidium is supported by two sterile basal cells up to µ m in width and has 1 6 sterile tip cells, or a short- to long-terminating trichome. The first sterile tip cells are µ m diameter (Figures 8, 11, and 12). Cystocarps oval, 280 µ m in width, 360 µ m in length, terminal on branchlets (Figures 9 and 13). Site and season of collection Wet season 7 11 December, 2007, La Mansi ó n, Punta Hansa and Rocky Cay. Known Caribbean distribution Belize, Cuba, Venezuela. Remarks The genus Nägeli encompasses approx imately 55 species, distributed in tropical and warm temperate waters (Masuda and Kogame 2000 ). The morphological characters discriminating among species include thallus size, branching pattern, number of pericentral cells, trichoblast morphology, among others (Masuda and Shimada 2002 ). However, these characters are often ambiguous either because many related species share the same features, or because some of the key characters vary intraspecifically (Masuda and Shimada 2002, Masuda et al. 2006, Garc í a et al ). For example, the number of pericentral cells may vary in different parts of the plant, ranging from 4 to 10 in the same specimen of tenella (C. Agardh) Ambronn (Masuda and Kogame 2000 ), and from 4 to 19 in crassa Hollenberg (Masuda et al ). In the original description of parca, Setchell (1926) mentioned that the alga had just 10 pericentral cells. However, later studies on the taxon by Hollenberg (1968) widened the range to 8 10 pericentral cells. The branching pattern d/d/d/i (d = determinate branch; i = indeterminate branch) is a key characteristic of H. parca, but it is also found in other species in the genus (i.e., delicatula Hollenberg,

5 M.R. Albis-Salas and B. Gavio: New algal records in Caribbean Colombia 541 Figures 8 13 parca. 8. Habit of male plant, showing spermatangial morphology. Scale bar = 100 µm. 9. Habit of female plant, showing position and morphology of cystocarp. Scale bar = 100 µm. 10. Tetrasporangial branches. Scale bar = 50 µm. 11. Detail of spermatangia with six terminal cells. Scale bar = 50 µm. 12. Spermatangia with a terminal short trichoblast. Scale bar = 30 µm. 13. Terminal, oval cystocarp. Scale bar = 50 µm. elongata M. Masuda & K. Kogame, pecten-veneris (Harvey) Falkenberg and H. tenella ). However, the pattern may vary in all species of (Schneider and Searles 1997 ), and we observed an increase in branching pattern variability when specimens were reproductive. Among structurally similar species, H. delicatula and H. pecten-veneris may be easily distinguished from H. parca by their branching at wide angles, which is not seen in H. parca. Furthermore, in H. pecten-veneris, the branching is distichous, a pattern very different from the one observed in H. parca (García et al ). In recent times, the morphology and position of reproductive structures have acquired new importance as taxonomic features (Masuda and Kogame 2000, Masuda and Shimada 2002, 2003, Masuda et al ). H. parca, H. elongata, and H. tenella have a very similar vegetative appearance, but can be distinguished by their reproductive structures (Masuda et al. 2006, Garc í a et al ). H. tenella has cystocarps inserted laterally on thickened branches, spiraled spermatangia with one or two sterile tip cells, and tetrasporangia per series (Masuda and Kogame 2000, Garc í a et al ). H. parca and H. elongata both have terminal cystocarps, but they may be easily separated by the thickened carpogonial branches of the latter, and by its very long terminal sterile tip on the apex of the spermatangia (Masuda and Kogame 2000 ). Furthermore, H. elongata produces 5 10 tetrasporangia per series, whereas in H. parca the number is reduced to 5 6 (Hollenberg 1968, Masuda and Kogame 2000, Masuda et al ). H. parca was originally described from the Pacific Ocean, where it commonly occurs (Hollenberg 1968 ). In the Caribbean, it has been reported for Belize (Littler and Littler 1997 ), Florida (Dawes and Mathieson 2008, Littler et al ), Cuba (Suarez 2005 ), and Venezuela (García et al ). Our specimens are in agreement with the description of H. parca made by other authors (Hollenberg 1968, Dawes and Mathieson 2008, Littler et al ), although the prostrate axes of our samples are significantly smaller than those of the specimens from the Pacific or other Caribbean sites (Table 1 ). García et al. (2008), in Venezuela, found individuals with slender prostrate axes, µ m diameter, which, however, are thicker than ours (50 55 µ m diameter). Abbott (1999) states that H. parca in Hawaii has mature cystocarps with a peaked ostiole, but apparently this feature has not been reported elsewhere. Although most authors report the spermatangial stichidia ending with 1 5 sterile tip cells or a short trichome, we observed, in the same individual, the presence of a few sterile tip cells, or a short to very long trichome (Figures 8, 11, and 12). Spermatangial tip morphology has been considered a key character in, and it has been used as one of the main features distinguishing

6 542 M.R. Albis-Salas and B. Gavio: New algal records in Caribbean Colombia Table 1 Morphological features of parca and related species. Branching pattern Determinate branch height (mm) Prostrate axis diameter ( µm) L/W proportion in the prostrate axis Erect axis diameter ( µm) L/W proportion in the erect axes Segment number in the determinate branches Number of trichoblasts elongata d/d/d/i To 3 tenella d/d/d/i parca (Pacific) d/d/d/i (2) (40) (90) < ( 2 0 ) 2 (3) parca (Caribbean) d / d / d / i To ( 2 0 ) 2 3 parca (our specimen) d/d/d/i Apex Cystocarp position and shape Thickening growth of cystocarp-bearing branches Spermatangial branches Number of tetrasporangia per branch Tetrasporangial dimensions ( µm) References elongata tenella parca (Pacific) parca (Caribbean) parca (our specimen) Truncate Terminal, urceolate Present Terminal, with 5 7 sterile tip cells or a long trichome Tapering blunt Lateral, in the middle portion of the branch, urceolate Truncate Terminal, globular to urceolate, with a beaked ostiole when mature Blunt-truncate Terminal, urceolate with a long ostiole Present Subterminal, with short sterile tip cells Absent Terminal, with 1 2 (5) sterile tip cells Absent With 1 5 sterile tip cells or a short deciduous trichome Truncate Terminal, oval Absent Terminal, with 1 5 sterile tip cells or a short to long trichome Masuda and Kogame (2000) (2) Taylor (1960), Hollenberg (1968), Masuda and Kogame (2000), Schneider and Searles (1991), Hollenberg (1968), Abbott (1999) To µ m Littler and Littler (2000), Dawes and Mathieson (2008), Garc í a et al. (2008) This study

7 M.R. Albis-Salas and B. Gavio: New algal records in Caribbean Colombia 543 H. elongata from other taxa (Masuda and Kogame 2000 ). However, the variability we observed indicates that this is not a good taxonomic character for the genus. Widespread species of have morphological variation among their geographic populations. For example, Masuda and Kogame (2000) report differences in Malaysian H. tenella, when compared with descriptions from other regions. Hollenberg (1968) observed differences in H. parca through its Pacific distribution. Whether these differences represent normal variability among geographically distant populations or represent a cryptic taxonomic diversity which has not been recognized needs to be further studied. Previous authors (Schneider and Searles 1997, Masuda and Kogame 2000 ) have pointed out the necessity of corroborating species boundaries and the validating characters used for taxonomy in the genus. Coupled morphological and molecular analyses are needed to clarify the status of several populations, including the Caribbean H. parca. Acknowledgments The authors are grateful to Sandra P é rez, Trisha Forbes, Elizabeth Galeano, the family Jay Padilla, Harley Bent, Samir Bent, Carlos Ballesteros, Jairo Medina, and Heins Bent for help in the field. We thank Omar Abril for assistance in managing Illustrator and Photoshop programs. Michael Wynne and Suzanne Fredericq confirmed some of the identifications of the species, for which we acknowledge. We thank Michael Wynne for kindly providing critical literature and improving the text. The project was developed with the research permit for biological collecting issued by CORALINA. This research was funded by the Universidad Nacional de Colombia, sede Bogot á, through the projects # and # , and by the Fundación para la promoción de la investigación y la tecnología, Banco de la Rep ú blica with the convenio # This work is contribution No. 364 of CECIMAR, Universidad Nacional de Colombia and Programa de Postgrado en Biología Línea Biología Marina. References Abbott, I Marine red algae of the Hawaiian Islands. Bishop Museum Press, Honolulu, HI. pp Barriga-Bonilla, E., J.I. Hern á ndez-camacho, I. Jaramillo, R. Jaramillo- Mej í a, L.M. Mora-Osejo, P. Pinto and P.M. Ru í z-carranza La Isla de San Andr é s. Contribuciones al conocimiento de su ecología, flora, fauna y pesca. Serie de publicaciones Universidad Nacional de Colombia, Bogot á D.C. pp B ø rgesen, F The marine Alg æ of the Danish West Indies, Vol. II. Part I. Rhodophyceae. Dansk Botanisk Arkiv 3 : Bula-Meyer, G Estado actual de la taxonom í a de las macroalgas marinas de Colombia. Bol. Ecotrópica 33 : Dawes, C.J. and A.C. Mathieson The seaweeds of Florida. University Press of Florida, Gainsville, FL. pp Díaz, J.M., D.I. Gómez-López, L.M. Barrios and P. Montoya-Maya Composici ó n y distribuci ó n de las praderas de pastos marinos en Colombia. In : (J.M. D í az, L.M. Barrios and D.I. Gomez- Lopez, eds) Las praderas de pastos marinos en Colombia: estructura y distribuci ó n de un ecosistema estrat é gico. Series de Publicaciones Especiales No. 10. INVEMAR, Santa Marta, Colombia. pp D í az-pulido, G. and G. Bula-Meyer Marine algae from the oceanic atolls in the Southwestern Caribbean (Albuquerque Cays, Courtown Cays, Serrana Bank and Roncador Bank). Atoll Res. Bull. 448 : Díaz-Pulido, G. and M. Díaz-Ruíz Diversity of benthic marine algae of the Colombian Atlantic. Biota Colombiana 5 : Garc í a, M., N. Gil and S. G ó mez Nuevos registros de parca y H. arcuata (Rhodomelaceae, Rhodophyta) para la costa de Venezuela. Ernstia 18 : Gavio, B., S. Palmer-Cantillo and J.E. Mancera Historical analysis ( ) of the coastal water quality in San Andr é s Island, SeaFlower Biosphere Reserve, Caribbean Colombia. Mar. Poll. Bull. 60 : Hollenberg, G.J An account of the species of the red alga occurring in the central and western tropical Pacific Ocean. Pacifi c Sci. 22 : IDEAM Datos de las variables clim á ticas de la isla de San Andr é s, Providencia y Santa Catalina. Santafé de Bogotá D.C, Colombia. pp. 70. IGAC San Andr é s y Providencia, aspectos geogr á ficos. Instituto geográfico Agust í n Codazzi, Bogot á, Colombia. pp Kapraun, D.F Notes on the benthic marine algae of San Andrés, Colombia. Carib. J. Sci. 12 : Littler, D.S. and M.M. Littler An illustrated marine flora of the Pelican Cays, Belize. Bull. Biol. Soc. Wash. 9: Littler, D.S. and M.M. Littler Caribbean reef plants. An identifi cation guide to the reef plants of the Caribbean, Bahamas, Florida and Gulf of Mexico. Offshore Graphics, Inc., Washington, DC. pp Littler, D.S., M.M. Littler and M.D. Hanisak Submersed plants of the Indian River Lagoon: A fl oristic inventory and fi eld guide. Offshore Graphics. Washington, DC. pp Masuda, M. and K. Kogame elongata sp. nov. and H. tenella (Rhodophyta, Ceramiales) from the western Pacific. Cryptogamie. Algol. 21 : Masuda, M. and S. Shimada Taxonomic notes on vietnamica (Rhodophyta, Ceramiales). Cryptogamie. Algol. 23 : Masuda, M. and S. Shimada A new red alga japonica (Rhodomelaceae, Ceramiales) from the Northwestern Pacific. Cryptogamie. Algol. 24 : Masuda, M., M. Tani and A. Kurihara Taxonomic notes on three species of (Ceramiales, Rhodophyta) found in Japan. Phycol. Res. 54 : Schneider, C.W. and R.B. Searles Seaweeds of the southeastern United States. Cape Hatteras to Cape Canaveral. Duke University Press, Durham, NC. pp Schneider, C.W. and R.B. Searles Notes on the marine algae of the Bermudas. 2. Some Rhodophyta, including Polysiphonia tongatensis and a discussion on the secunda/ tenella complex. Cryptogamie. Algol. 18 : Schnetter, R Marine Algen der karibischen K ü sten von Kolumbien I: Phaeophyceae. Bibliotheca Phycol. 24 : Schnetter, R Marine Algen der karibischen K ü sten von Kolumbien II: Chlorophyceae. Bibliotheca Phycol. 42 : Setchell, W.A Tahitian algae and Tahitian Spermatophytes. Univ. Calif. Publ. Bot. 12 : Suarez, A.M Lista de las macroalgas marinas cubanas. Rev. Invest. Mar. 26 : Taylor, W.R Algae collected on the Presidential Cruise of Smithsonian Misc. Coll. 98 : Taylor, W.R Marine algae of the eastern tropical and subtropical coasts of the Americas. University of Michigan Press, Ann Arbor, MI. pp Received 8 July, 2011; accepted 16 November, 2011