Polychaetes of the mangrove-fouling community at the Colombian Archipelago of San Andrés and Old Providence, Western Caribbean
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1 Wetlands Ecology and Management 10: , Kluwer Academic Publishers. Printed in the Netherlands. 227 Polychaetes of the mangrove-fouling community at the Colombian Archipelago of San Andrés and Old Providence, Western Caribbean Mario Londoño-Mesa 1,JaimePolanía 2 &ImeldaVélez 3 1 Departamento de Ecología Acuática, El Colegio de la Frontera Sur-ECOSUR, Apartado Postal 424 Chetumal QR Mexico, Tel: (983) , mariol@ecosur-qroo.mx; 2 Universidad Nacional de Colombia Sede San Andrés, Carretera Circunvalar de San Luis, Sector Free Town #52-44, San Andrés Isla, Colombia, Tel: 57(8) , Fax: 57(8) , jhpolanv@dnic.unal.edu.co; 3 Departamento de Biología, Universidad de Antioquia, Calle 67 5# Of, 233, Medellín, Colombia, Tel & Fax: 57(4) , ivelez@matematicas.udea.edu.co Key words: associated fauna, communities, mangrove roots, Polychaeta, Western Caribbean Abstract This study records the polychaetes found on the submerged roots of Rhizophora mangle on San Andrés and Providence Islands, Colombian Caribbean. Sampling was done in 1998 during the rainy (July) and dry (November) seasons; each season, 17 roots were collected in three different stations with different kinds of human impact, two in San Andrés and one in Providence. At the same time temperature, salinity and dissolved oxygen were measured in situ. Aromatic hydrocarbons were measured in the laboratory. The polychaetes were removed from the roots and identified. The available root area for the organisms was also measured. Five genera and 11 species were newly recorded for the Colombian Caribbean. The most abundant families were Terebellidae in Old Providence Mc Bean Lagoon, Syllidae in Honda Bay and Nereididae in Hooker Bay on the San Andrés Island. Thelepus setosus (Terebellidae) and Amblyosyllis sp. (Syllidae) were highly abundant in less polluted sampling stations such as Old Providence Mc Bean Lagoon and Honda Bay. On the other hand, Neanthes succinea (Nereididae) were abundant in Hooker Bay which was the most polluted station. Salinity seemed to be the most important parameter for the polychaete populations. The populations of polychaetes, as a total group, seemed to be related to the root area available on both islands, independent of the season. However, during the rainy season, the populations were independent of root area availability, while during the dry season, the populations were dependent on it. Introduction Mangrove forests are important tropical coastal ecosystems, since they serve as an interface between the land and sea, producing high levels of nutrients and providing habitats for a great number of molluscs, crustaceans and fish with commercial importance that, in turn, support human populations (Rützler and Feller, 1996). The submerged roots of the red mangrove, Rhizophora mangle, serve as substratum for a large number of crust-forming, boring and vagile marine organisms, which form subsystems with their own organization, structure and dynamics (Reyes and Campos 1992). The mixed waters and the exceptional abiotic conditions of the mangroves produce their benthic communities high diversity, remarkable organization level (Prahl et al., 1990) and are important for energy and matter flow between habitats. Colombia possesses some hectares (ha) of swamps (Lacerda, 1993), on both the Caribbean (20 30%) and Pacific coasts (70 80%). Recent studies have been limited to the continental Caribbean coast, disregarding the San Andrés and Providence oceanic archipelago. A pioneer study on San Andrés Island (Barriga-Bonilla et al., 1969) characterized the ecosystem and recorded some crustaceans, echinoderms and fishes.
2 228 Inside this ecosystem, the polychaetes are a valuable source of food, being mainly benthic and inhabiting areas from the intertidal zone to oceanic depths (Amaral and Nonato, 1981). They have been the basis of several environmental studies, useful for the determination of lethal pollutants and are good indicators for the acute, chronic and sublethal effects of contamination (Salazar-Vallejo et al., 1989). Salazar- Vallejo (1996b) listed 1240 polychaete species for the Great Caribbean Region (from South Carolina and the Gulf of Mexico to the Brazilian central coast), including the islands considered in this study. In his view, however, these figures represent only a third of the total potential annelids existing there. Cosmopolitan and endemic species have been registered for both Colombian coasts; Laverde-Castillo (1986) recorded 94 species for the Colombian Pacific coast, and Dueñas (1999) recorded 145 species for the Caribbean, including some data from Providence Island. The recognition of more species allows for more in-depth ecological studies of the existing habitats, their roles in the ecosystem, water quality, etc. Because mangroves are under great pressure by deforestation, landscape transformation and decrease of fresh water inputs, more studies of this important ecosystem are needed. The purpose of this work is to improve our knowledge of polychaete populations associated with red mangrove roots on San Andrés and Providence Islands, and their relationship with some physical and chemical parameters. At the same time, the aim is to increase the amount of faunal information for the Great Caribbean Region. This study was part of the project Evaluación preliminar de la Biodiversidad Marina Asociada a los Manglares del Parque McBean Lagoon en Providencia y Bahías Honda y Hooker en San Andrés, Caribe Colombiano (Santos-Martínez et al., 1998b). Method The San Andrés and Providence Archipelago is located 800 Kilometers (km) northwest off the Colombian coastline and 150 km off Nicaragua. San Andrés is 95 km south of Old Providence. The area is characterized by a tropical climate dominated by trade winds, with a dry season between January and April and a rainy season starting in May-July, with a peak in November (Diaz et al., 1995). Honda and Hooker Bays on San Andrés are located on the northeast coast. The former has 34.4 ha of riverine mangrove at its north end projecting into the adjacent Hooker Bay (Angel, 1998). In Honda Bay, sea grasses and macroalgae are found in the same area; the site is partially stressed, since some sewage drains into its waters. In turn, Hooker Bay has a 15.1 ha R. mangle fringing mangrove; it was an open shallow inlet but as a consequence of massive dredging and several activities related to a former power plant, it is now a semi-enclosed water mass with restrained circulation. The ecosystem has undergone a chronic accumulation of hydrocarbons in the sediments, among other stresses (García and Gaviria, 1996). Old Providence McBean Lagoon Natural National Park, located in the east sector of Providence Island, possesses a large fringing mangrove, with ca. 27 ha located behind the barrier reef. The productivity of the ecosystem is highly dependent on sediments brought in by natural stream drainage, which form a large and low shelf (Skinner, 1994). The National Park is free of direct human impact. The surveys were carried out during July, 1998, at the end of dry season, and during November 1998, at the peak of the rainy season, according to Santos- Martinez et al. (1998ab). Each collection comprised 5 roots from Honda and Hooker Bays, and 7 roots from McBean Lagoon. These samples were taken according to spatial gradient of pollutants originating from the nearly population, and towards the outside of the bay; the former was regarded as the region with a direct influx of pollutants. In the field, each root (submerged but not anchored) was covered with a plastic bag to avoid mobile species losses. The roots were then cut above the high tide level. The bag was labeled, sealed and refrigerated. The length and diameter of each root was noted in the laboratory, and by a Spearman s Correlation coefficient (p = 0.05), they were compared with the quantity of polychaetes found on each one. Polychaetes were sorted, fixed in neutralized 10% commercial formaldehyde solution in seawater and preserved in 70% ethanol. The worms were identified following Åkesson and Rice (1992), Carrera- Parra and Salazar-Vallejo (1998), Dueñas (1979), Eibye-Jacobsen and Møbjerg-Kristensen (1994), Estapé and San Martin (1991), Fauchald and Reimer (1975), Fauchald (1977ab, 1992), Harper (1971), Hartman (1951), Jiménez-Cueto and Salazar-Vallejo (1997), Liñero (1985, 1991), Liñero and Reyes (1979), Nonato and Amaral (1979), Nonato and Luna (1970),
3 229 Table 1. Available area of R. mangle roots and polychaete numbers for the three sampling sites in San Andrés and Providence Islands, Colombian Caribbean, during July and November Hooker Honda McBean Total Bay Bay Surface (m 2 ) N. Individuals Salazar-Vallejo (1996ab), Salazar-Vallejo and Carrera- Parra (1998), Salazar-Vallejo et al. (1989) and Smith (1964). A NIKON microscope was used for the smallest structures, and a WILD M3 Stereomicroscope with a Drawing Camera was used to draw larger structures. A list of species in each place was prepared with their quantitative descriptions. The procedure ended up with a comparative analysis of the studied areas using density (individuals per root). Salinity, temperature and dissolved oxygen were measured in situ for each case. Aromatic hydrocarbons were measured in the laboratory of National University of Colombia, at San Andrés. The concentrations of total aromatic hydrocarbons in sediments were measured only in July. Months and sample sites were compared by a simple coefficient of variation. A two-way ANOVA was used to analyze differences between sites, months with salinity, temperature and dissolved oxygen; moreover, a one-way ANOVA was used for aromatic hydrocarbons because they were measured only in July. These statistical analyses were possible with STATGRAPHICS Version 7.0. Results Available area and quantity of worms for each sampling site is showing in Table 1. According to these data, a value of (coef. of 0.047, p = 0.05 Spearman s) demonstrated the independence between the polychaete community recorded and the available area per root, in any climatic season. In contrast, for July, a value of (coef. of 0.412, p = 0.05) showed that the number of individuals depended on the available area in each of the three studied sites. It did not occur in November, where a value of showed no dependence on the area. From 1962 worms, 49 species were identified (Table 2). Five genera and 11 species are newly recorded for the Colombian Caribbean (indicated by ). Table 2. Number of individuals of polychaete species associated with mangrove roots in Providence McBean National Natural Park (NNP), and Hooker and Honda Bays in San Andrés Island, Colombian Caribbean, in July and November, ( new records for the Colombian Caribbean). Taxa McBean Honda Bay Hooker Bay July Nov. July Nov. July Nov. Amblyosyllis sp Branchiosyllis sp Branchiosyllis sp Branchiosyllis sp Opistosyllis brunnea Syllis gracilis Syllidae IND Trypanosyllis sp Typosyllis variegata Typosyllis sp Ceratonereis sp Ceratonereis irritabilis Leptonereis sp.? Neanthes succinea Nereis riisei Stenonereis sp.? Tylorrhynchus bahamensis Branchiomma nigromaculata Branchiomma sp Megalomma lobiferum Sabellidae IND Streblosoma bairdi Terebellidae IND Thelepus setosus Eunice antennata E. atlantica E. cariboea E. denticulata E. filamentosa E. tridentata Lysidice ninetta Marphysa aransensis M. longula Marphysa sp Marphysa sp Nematonereis unicornis Nematonereis sp Palola sp Polynoidae IND Maldanidae IND Lumbrineridae IND Lumbrineris sp.? Sigalionidae IND Terebellides stroemi Dorvillea sociabilis Polydora cf. websteri Fam Fam Fam Individuals Species
4 230 We have to keep in mind that sampling errors cannot be dismissed due to problems identifying fragmented organisms. The individuals corresponding to three families could not be identified because of their bad condition. These problems emerged due to the freezing method used and the time that it took whilst the roots were sorted. Moreover, at the moment of extracting worms, many of them were strongly attached to the root and they were fragmented. Thus, a genus record of the name of each family both known and unknown was taken. In July the largest number of individuals of Thelepus setosus" (Terebellidae) were found on root 1, with, 204 individuals, and root 2, with 154. The species Branchiomma nigromaculata and Megalomma lobiferum (Sabellidae) were also present in high numbers in the roots 2 and the 5, respectively. In November also many individuals of T. setosus occurred (308 in root1and188inroot7), while M. lobiferum was well represented as well (data not shown). In Honda Bay Amblyosyllis sp. (Syllidae) occurred in July with more individuals (36) than any other species, followed by Branchiosyllis sp.1 (Syllidae) with 27 individuals. However, the former was present only on a single root (root 4), while the latter was found in all except one root (root 5). In November Branchiosyllis sp.1 was again the most dominant species (16 individuals for root 4 and 27 for root 5), while 10 more individuals of B. nigromaculata and none of Amblyosyllis sp. were counted. In Hooker Bay during July, the dominant species were Neanthes succinea (Nereididae) with 40 individuals (root 1), Streblosoma bairdi (Terebellidae; 31 individuals in root 5), Polydora cf. websteri (Spionidae; 21 in root 2), and B. nigromaculata (20 individuals in the root 5). N. succinea occurred in four out of five roots, while very few individuals of P. cf.websteri were present in root 4. In November N. succinea had the largest quantity of individuals in each of the roots (58 in root 1, 36 in root 4, and 17 in root 5). As shown in Table 3, the largest temperature fluctuations, represented as a major coefficient of variation (between parenthesis), were recorded in Hooker Bay during July, while McBean and Honda Bay produced intermediate and low values, respectively. Nevertheless, the highest average value was measured in Mc- Bean. Temperature was very homogeneous throughout the two seasons although it was slightly higher in November, and also higher for inner lagoons than wave exposed areas (Data not shown). Salinity measures had high coefficient values in Hooker Bay, while McBean had the lowest average values during July (Table 3). Also in Hooker Bay, the salinity values were the lowest, in contrast to McBean, where the high values were recorded. During November, salinity was higher in Honda Bay, despite it being the rainy season. The highest average value of dissolved oxygen was recorded in Hooker Bay, whilst the major variation was presented in McBean, corresponding to November. Aromatic hydrocarbon was the parameter that presented the highest values about the coefficient of variation. Hooker Bay showed an elevated value of , indicating possible problems in measurements or in sea environment. In contrast, Honda Bay recorded the lowest value, although it was also high compared to the others parameters. On the other hand, the two-way analysis of variance (p = 0.05) showed that temperature was not significant for both sites and months (Table 4), although the relation with the month is close to being significant (0.0549). Salinity and dissolved oxygen were significant, but comparing them, the salinity was closer to zero, indicating that that is the most important parameter to analyze. Finally, the one-way analysis corresponding to aromatic hydrocarbons showed a very high value, being particular significant for July. Discussion In both islands, the community of polychaetes seems to be a function of the available root area rather than being related to the season. However, during the rainy season the population seems to be independent of the availability of root area, and it depends on some unidentified environmental factor. According to the associated fauna found in the roots, sponge and alga cover seem to affect the polychaete community negatively, because when these groups appeared, no worms were extracted. Five genera and 11 species were newly recorded for the Colombian Caribbean sea, according to the checklist made by Dueñas (1999). Nevertheless, these identifications need to be corroborated in the future because of the bad condition of some worms. Moreover, it has to be taken into account that many species reported for the Caribbean region are based on taxonomical erroneous information due to the lack of catalogues or standardized information. Thus, it could be that the
5 Table 3. Temperature, salinity, dissolved oxygen and concentration of aromatic hydrocarbons in Old Providence McBean National Natural Park (NNP), Providence Island, and Honda and Hooker Bays, San Andrés Island, Colombian Caribbean, during July (The values are averages with the standard deviation; coefficient of variance between parenthesis, and for the highest and for the lowest values). Sites Month Temp. Salin. Diss. Oxygen A. Hydro. ( C) ( ) (mgo 2 l 1 ) (µg g 1 ) McBean Lagoon July 30.14±0.9 (2.98) 35.14±1.57 (4.48 ) 7.46±0.65 (8.79) 1.036±1.27 (123.00) Nov ±0.63 (2.17) 32.42±4.16 (12.82) 6.70±1.72 (25.77 ) Honda Bay July 26.50±0.5 (1.89) 33.62±1.91 (5.70) 5.92±0.48 (8.14 ) 1.096±0.35 (32.28 ) Nov ±0.58 (2.01) 34.00±2.83 (8.32) 6.52±1.24 (19.08) Hooker Bay July 27.42±1.00 (3.61 ) 11.20±5.54 (49.47 ) 4.18±0.83 (19.97) 0.516±0.73 ( ) Nov ±0.48 (1.64 ) 25.70±1.72 (6.68) 11.30±1.51 (13.39) 231 names of some species we record here do not correspond to real species. In the future, this material will be available for other studies. Thelepus setosus and Amblyosyllis sp. were species highly represented in sampling stations little affected by pollutants, with less variable salinity and temperatures, such as McBean and Honda Bay. In addition to this, dissolved oxygen levels were more variable showing significant values in McBean, which could indicate that the biological and chemical activity along the coast allow the establishment of great numbers of animals, namely terebellids and syllids in this instance. On the other hand, N. succinea was highly abundant in Hooker Bay, where the hydrocarbon variability was the highest. Nevertheless, this fluctuation could be influenced by the season, because the parameters were only measured in July, and nothing is known about November. Thus, it will be useful to compare this value with others from the same area to be more informed about the process. Hooker Bay also presented major variances and significant levels relating to temperature and salinity. At the moment, it seems that N. succinea could be considered an indicator species for polluted and shallow waters, associated to submerged mangrove roots. Based on the data processed, the good environmental conditions in McBean, as a National Natural Park, is reinforced with this study. Thus, the role of mangrove forests as a highly productive ecosystem, but ecologically weak, is the reason for protecting it and management programmes have to begin with the study of their associated fauna. After this study, the importance of polychaetes as biological indicators will continue to increase, and we hope that this study will be the framework for further studies on polychaetes. Table 4. Two-way ANOVA showing differences between sites, months and physical chemical parameters. Source of Temp. Salin. Diss. A. Hydro. variation Oxygen Sites Months Interaction Acknowledgements The authors thank the Comité para el Desarrollo de la Investigación, Universidad de Antioquia for funding the travel of M. Londoño to San Andrés Island. A COLCIENCIAS grant and financial aid from San Andrés Station from Universidad Nacional de Colombia were necessary to do the samplings. Adriana Santos-Martinez led the main project. M. Londoño-Mesa thanks Sergio I. Salazar- Vallejo, from El Colegio de la Frontera Sur, Mexico, for the taxonomic keys and advice about the manuscript; Jenny Ruiz-Ramirez for the keys on exogonid Syllids from the Great Caribbean, John. J. Ramirez for revising the manuscript and for his valuable help with the equipment. P.R. Dueñas, Universidad de Córdoba, for the taxonomic keys and suggestions, S. Vilardy for thedataprocessing. References Åkesson B. and Rice S Two new Dorvillea species (Polychaeta, Dorvilleidae) with obligate asexual reproduction. Zoologica Scripta 21(4): Amaral, A.C. and Nonato, E.F Anelídeos Poliquetos da Costa Brasileira: Características e chave para famílias-glossário. Conselho Nacional de Desenvolvimiento Científico e Tecnológico: Brasilia, 47 pp.
6 232 Angel, I.F Estructura y Distribución de las Praderas de Fanerógamas Marinas en la Isla de San Andrés, Caribe Colombiano. BSc. [monography]. Universidad Jorge Tadeo Lozano. Bogotá, 188 pp. Barriga-Bonilla, E., Hernández-Camacho, J., Jaramillo, I., Jaramillo-Mejía, R., Mora-Osejo, L.E., Pinto-Escobar, P. and Ruiz-Carranza, P.M La isla de San Andrés: Contribuciones al conocimiento de su ecología, flora, fauna y pesca. Instituto de Ciencias Naturales Facultad de Ciencias de la Universidad Nacional de Colombia. Dirección de Divulgación Cultural, Bogotá D.E. 152 pp. Carrera-Parra, L.F. and Salazar-Vallejo, S.I (1997). Eunícidos (Polychaeta) del Caribe mexicano con claves para las especies del Gran Caribe: Eunice. Rev. Biol. Trop. 45(4): Díaz, J.M., Garzón-Ferreira, J. and Zea, S Los arrecifes coralinos de la isla de San Andrés, Colombia: Estado actual y perspectivas para su conservación. Academia Colombiana de Ciencias Exactas, Físicas y Naturales. 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Instituto de Estudios Caribeños Sede San Andrés Universidad Nacional de Colombia, 16 pp. Skinner, A Moluscos y Crustáceos Asociados a los Manglares de las Islas de Providencia y Santa Catalina. BSc. [monography]. Universidad del Valle. Cali, 183 pp. Smith, R Key to marine invertebrates of the Woods Hole Region. Systematic Ecology Program, Marine Biological Lab. Massachusetts Contribution 11:
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