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The Caribbean Coastal Marine Productivity Program (CARICOMP) was launched in 1993 to study regional long-term interactions between land and sea, taking standardized measurements of productivity and biomass of mangroves, coral reefs and seagrasses. Since 1999 continuous measurements of seagrass (Thalassia testudinum) parameters as well as environmental data have been recorded in Caribbean Panama. Replicate stations were selected near the ]]>
2/d, 66.6gDW/m2, 2.62%/d, 1 481 gDW/m2, and 4.65, respectively. Total dry biomass (shoots, rhizomes and roots) and LAI of T. testudinum increased significantly during the study period. Mean values for total rainfall, Secchi disk depth, sea surface temperature, ]]>
T. testudinum may be linked to ocean ]]>
T. testudinum population, increasing respiratory demands and microbial metabolism.
Key words: Caribbean, Panama, CARICOMP, time-series, productivity, Thalassia testudinum.
Resumen
El Programa de ]]>
Thalassia testudinum) así como datos ambientales han sido registrados para el Caribe de Panamá. Réplicas de estaciones fueron seleccionadas cerca del Instituto Smithsonian de Investigaciones Tropicales en Bocas ]]>
2/d, 66.6gDW/m2, 2.62%/d, 1 481 gDW/m2, y 4.65, respectivamente. La biomasa total seca (haces, rizomas y raíces) e Índice de Área Foliar de T. testudinum incrementaron significativamente durante el periodo de ]]>
T. testudinum (biomasa total y LAI) fueron tanto positivos como significativos. La población humana ha crecido dramáticamente durante los últimos diez años en la ]]>
T. testudinum pueden estar ligados al calentamiento oceánico, como una consecuencia para satisfacer los requerimientos metabólicos de la planta, aunque es necesario analizar otros factores locales (reducción del pastoreo e incremento en la eutrofización). Un mayor calentamiento del océano puede tener efectos negativos en la población de ]]>
T. testudinum, incrementando las demandas respiratorias y el metabolismo microbiano.
Palabras clave: Caribe, Panamá, CARICOMP, series temporales, productividad, Thalassia testudinum. ]]>
Seagrass meadows are a key ecosystem of the coastal zone, they are highly productive, fixing 15% of the carbon fixed by all oceanic primary producers (Duarte & Chiscano, 1999). Play a fundamental role as nursery and refuge for fish and other marine species (Verweij, Nagelkerken, De Graaff, Peeters, Bakker, & Van der Velde, 2006; Heck Hays & Orth, 2003), enhance diversity (Casares & Creed, 2008), are a source of food for ]]>
Worldwide, seagrass habitats have decreased for more than three decades (Orth, Carruthers, Dennison, Duarte, Fourqurean, & Heck, 2006; Short, Polidoro, Livingstone, Carpenter, Bandeira, & Bujang, 2011) and the current habitat loss ]]>
2/y, this is a dramatic increase considering that between 1879 and 2006 the decrease rate was estimated at 27km2/y (Waycott, Duarte, Carruthers, Orth, Dennison, & Olyarnik, 2009). This loss has been attributed mostly to human development of the coastal zone, which poses threats such as dredging, housing development, and boat traffic (Short & Burdick, 1996, Erftemeijer & Robin Lewis, 2006, Björk, Short, Mcleod, & Beer, 2008; Halpern, Walbridge, Selkoe, Kappel, Micheli, & ]]>
Thalassia testudinum (Banks ex König) which covers and approximate area of 2 790km2 (Green & Short, 2003), although the most recent estimate (Wabnitz , Andréfouët, Torres-Pulliza, Müller-Karger, & Kramer, 2008) set the seagrass extension for the wider Caribbean at almost 70 000km2. In Caribbean Panama, human pressure on coastal ecosystems continues to build through deforestation ]]>
et al., 2012).
Many economic and cultural ]]>
et al., 2008). The need for long-term monitoring is crucial to evaluate possible impacts of human and natural disturbances. In 1993 the Caribbean Coastal Marine Productivity Program (CARICOMP) was launched to study regional long-term interactions ]]>
et al., 2001, CARICOMP, 2001). As a result of this project, information of turtlegrass meadows from different regions of the Caribbean has been published. It was found that nutrient enrichment is having a negative effect on T. testudinum, decreasing its coverage and biomass in Bon Accord Lagoon, Tobago (Juman, 2005). Fonseca, Nielsen, & Cortés (2007) reported a decrease in both biomass and productivity as a consequence of ocean warming in Cahuita National Park, Costa Rica, from 1999 to 2005, with ]]>
T. testudinum population. Murdoch, Glasspool, Outerbridge, Ward & Gray (2007) analyzed data from 1962 to 2004 and found a widespread decline in Bermuda meadows located at the rim of the reef and in the lagoon, while inshore and nearshore meadows remain relatively constant. A similar result was published by Krupp, Cortés, & Wolff (2009) for Cahuita National Park, stating that although turtlegrass meadows are in good health, it is probable that they are at their maximum level of tolerance for environmental ]]>
Data for Caribbean Panama has not ]]>
T. testudinum to evaluate the variability of: above-ground biomass (shoots), below-ground biomass (rhizomes and roots), standing crop, Leaf Area Index (LAI), leaf productivity and turnover rate. Possible correlations between environmental variables (seawater temperature, salinity, total ]]>
Materials and Methods
Study area: ]]>
T. testudinum) meadows at the CARICOMP site in Isla Colon extend from the shore into the sea to a distance of 150m. The CARICOMP monitoring site is near the Smithsonian Tropical Research Institute (STRI) facilities on Isla Colon in the Bocas del Toro Archipelago (9°21’0" N - 82°15’0" W). The Archipelago lies along the Northwest Caribbean coast of Panama and is formed by numerous forested islands and two major semi-enclosed basins: Bahía Almirante, the location of the study site, and Laguna de Chiriquí. Rainfall in the area is ]]>
Bahía Almirante is a relatively small lagoon (446km2) with coarse sand, carbonate-dominated ]]>
et al., 2005, D’Croz et al., 2005). Land clearing for agricultural and cattle rearing purposes or timber commodities has increased the amount of nutrient runoff into Bahía Almirante and reduced water quality in the last four decades with consequences for reef-building corals (Guzman, 2003; ]]>
et al., 2005) according to the water quality levels reported by Green & Webber (2003).
Circulation inside Bahía ]]>
Fig. 1, Guzman, Barnes, Lovelock, & Feller, 2005). Seawater temperature inside Bahía Almirante fluctuates throughout the year in relation to the amount of solar radiation reaching the sea surface (Kaufmann & Thompson, 2005). Main primary producers in the shallow (<3m) and deeper (up to 15m) parts of Bahía Almirante are the seagrass
T. testudinum and corals such as Agaricia tenuifolia (Guzman & Guevara, 1998).
Seagrass data: Two research stations were located in Bahía Almirante, 12 to 18m from the shore and less than 60m apart from each other (9°21’0" N - ]]>
Fig. 1, Guzman et al., 2005). For a detailed description of the sampling methods refer to CARICOMP (2001). A brief description of these methods is provided below. Turtlegrass sampling began in March 1999 and is ongoing (for this work we included until January 2010). In order to assess the local seasonal signature, sampling interval was more intense during the first campaigns, with four sampling events per year in 1999 (February, June, September, December) and three in 2000 and 2001 (January, July, October). Analysis ]]>
Core sampling: Thalassia testudinum ]]>
Quadrant sampling: Productivity samples were measured with a PVC quadrant (10x20cm). All turtlegrass shoots inside the quadrant were perforated 2mm above the sheath with a syringe needle to measure growth (an average of 18 shoots per quadrant). Marked leaves were left to grow for six to eight days, after that all shoots were harvested for further processing. Leaves were separated in three categories according to growth status (new leaves, growth on old leaves, and old leaves). Growth (productivity), standing crop (leaf biomass) and turnover rate (leaf percentage replaced daily) ]]>
2) returns the LAI, which is a descriptor of ]]>
Environmental data: Seawater surface temperature (SST), salinity and Secchi disk depth (horizontal measurements) were recorded above a seagrass meadow (average depth 2m) near the CARICOMP site (9º21’0"N-82º15’0"W). A handheld YSI 85® was used for the salinity measurements (0.5m depth), while ]]>
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Time-series processing and statistical analyses were performed with SigmaPlot 10®. Except for the rainfall data, monthly means were calculated for each time series. Normality and equal variance were tested using Kolmogorov-Smirnoff and Levene Median statistics, respectively. Standard error and the plotted anomaly of each time series assisted in the identification of periods of highest variability. Non-parametric Spearman Rank Correlation analyses were applied to: i) identify significant inter-annual trends for each time series; ii) determine significant correlations between ]]>
Results
Productivity and ]]>
T. testudinum:Growth (1999-2010) in Bocas del Toro had a mean value of 1.74gDW/m2/d, ranging from 1.07 to 5.80gDW/m2/d (Fig. 2A). Productivity did not show a statistically significant (p>0.05) trend with time; however, productivity values were above 6.0gDW/m2/d only after 2003 (Fig. 2A). The decadal mean for standing crop (leaf biomass) was ]]>
2. No significant (p>0.05) trend in standing crop was detected over the sampling period (Fig. 2B); minimum (55.54gDW/m2) and maximum (94.04gDW/m2) values corresponded to July 2004 and February 2007, respectively. Turnover rate mean (1999-2010) for the leaves of Thalassia testudinum was ]]>
Fig. 2C). Although no significant (p>0.05) trend was observed, before 2002 leaf percentage replaced daily were below 4.0%/d; in contrast, turnover rate frequently exceeded 7.0%/d after 2002. Total biomass (leaves, shoots, rhizomes and roots) decadal mean was 1 481gDW/m2, ranging from 916gDW/m2 (June 1999) to 2 129gDW/m2 (January 2008). Total biomass showed a ]]>
Fig. 2D). At the beginning of the time series, maximum total biomass values were 1 793gDW/m2 (March 1999) and 1 802gDW/m2 (June 2000), whereas at the end of the time series maximum values were over 40% higher, 2 521gDW/m2 (June 2006) ]]>
2 (January 2009). The decadal mean of LAI was 4.65 (range, 3-7), with values over 19 after 2002 (Fig. 2E). Leaf Area Index showed a significant increase with time (p=0.0139, r=0.47, df=25), however, lower than the correlation observed for total biomass (Fig. 2D). ]]>
Environmental variables: With the exception of seawater surface temperature (SST), none of the environmental variables measured between 1999 and 2010 exhibited a significant (p>0.05) correlation with time (Fig. 1). SST demonstrated a significant increase (p=0.000, df=89 318) over time, with a low Spearman Rank Correlation coefficient (r=0.09).
Mean total rainfall was 3 498mm (1999-2010), highest values occurred in November-December, while the lowest occurred in September-October (Fig. 3A). Mean Secchi depth was 8.24m, with maximum and minimum visibility in March (10m) and August (6m), respectively (Fig. 3B). ]]>
Fig. 3C). Salinity decadal mean value was 32.26psu, with three episodes of extremely low salinity (<25psu) that coincided with periods of intense rainfall (May 2002, December 2004, and December 2008) (Fig. 1A, D). ]]>
Time-series correlations: Total rainfall was negatively correlated with SST (p=0.0043, r=-0.25, df=128) and both variables were significantly correlated with salinity (rainfall: p=0.000, r=-0.47, df=125, SST: p=0.0056, r=0.25, df=125, respectively, Table 1). Moreover, water column visibility was positively correlated with SST (p=0.0199, r=0.21, df=126) and salinity ]]>
T. testudinum parameters. Standing crop and growth were positively correlated with SST (standing crop: p=0.0065, r=0.51, df=25, growth: p=0.0459, r=0.39, df=25, respectively), whereas water column visibility was negatively correlated with LAI (p=0.0173, r=-0.47, df=23).
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Discussion
The environmental and biological data reported herein are a contribution to the long time-series that has been published as part of the CARICOMP project (Juman, 2005; Murdoch et al., 2007; Cortés, Fonseca, Nivia-Ruiz, ]]>
et al., 2012). Human population of Bocas del Toro has increased dramatically over the last ten years (Trombulak, 2006), leading to destruction of several hectares of mangrove forests and the lack of a sustainable urban plan for wastewater disposal (Trombulak, 2006).
There was an increase in total ]]>
T. testudinum from 1999 to 2010 in Bocas del Toro which could be a result of seawater temperature increase in the last decade. Positive correlation between SST with productivity (p=0.046, r=0.39, df=25) and standing crop (p=0.007, r=0.51, df=25) also support this hypothesis. Leaf Area Index increase is possibly a result of the increase in total biomass, to satisfy the metabolic requirements for plant growth (Enríquez & Pantoja-Reyes, 2005). Lee, Park & Kim (2007) report that optimum temperature for growth and photosynthesis for T. ]]>
is 29°C, almost the average temperature recorded in our time series (28.79°C). Therefore, a further warming of the ocean could have a negative effect on turtlegrass meadows. Higher temperatures will increase their respiratory demands as well as microbial metabolism (Short & Neckles, 1999; Duarte, 2002), this will favor the occurrence of anoxic conditions in the sediment (Borum, Pedersen, Greve, Frankovich, Zieman, & Fourqurean, 2005). Also algal communities that already form part of the seagrass community might be benefited from this temperature increase, their overgrowth will limit the amount of light reaching the ]]>
These scenarios are exacerbated given the presence of eutrophic conditions. Eutrophication as a consequence of coastal runoff constitutes a potential threat to turtlegrass productivity (Van Tussenbroek, Vonk, Stapel, Erftemeijer, Middelburg, & Zieman, 2006). Fourqurean, Powell, Kenworthy, & Zieman (1995) found that fertilization of turtlegrass meadows had a ]]>
Halodule wrightii) standing crop of T. testudinum drastically dropped. Eutrophication also promotes abnormal phytoplankton blooms and macroalgae overgrowth which cannot be offset by fish-grazing (Gacia, Littler, & Littler, 1999). Nutrient enrichment can also displace T. testudinum by other seagrass species (Tomasko & Lapointe, ]]>
et al., 2006; Van Tussenbroek, 2011).
The increase in biomass recorded during the last decade and the associated temperature increase are evidence of the progressive changes occurring in the Caribbean, ]]>
et al., 2006; Ogden, 2010; Rodríguez-Martínez et al., 2010, Cramer et al., 2012). Land clearing activities, overfishing, global ]]>
et al. 2010, Cramer et al., 2012). It is imperative to continue efforts focused on mapping aereal extent of meadows (Wabnitz et al., 2008), its population dynamics (extension of vegetative genets and dispersal of sexual propagules), public awareness of the economic importance of healthy ecosystems ]]>
et al., 2002; Tibbets, 2006) to foster integrative national management and conservation plans for the upcoming environmental changes.
Acknowledgments
Authors wish to ]]>
References ]]>
Alcolado, P. M., Alleng, G., Bonair, K., Bone, D., Buchan, K., & Bush, P. G. (2001). The Caribbean Coastal Marine Productivity Program (CARICOMP). Bulletin of Marine Science, 69(2), 819-829. [ Links ]
Aronson, R. B., MacIntyre, I. G., Wapnicks, C. M., & O’Neill, M. W. (2004). Phase shifts, alternate states and the unprecedented convergence of two reef systems. Ecology, 85(7), 1876-1891. [ Links ]
Bachelet, G., Montaudouin, X., Auby, I., & Labourg, P. J. (2000). Seasonal changes in macrophyte and macrozoobenthos assemblages in three coastal lagoons under varying degrees of eutrophication. ICES Journal of Marine Science, 57, 1495-1506. [ Links ]
Björk, M., Short, F., Mcleod, E., & Beer, S. (2008). Managing seagrasses for resilience to climate change. Gland, Switzerland: IUCN. [ Links ]
Borum, J., Pedersen, O., Greve, T. M., Frankovich, A., Zieman, J. C., & Fourqurean, J. W. (2005). The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. Journal of Ecology, 93, 148-158. [ Links ]
Burkholder, J. M., Tomasko, D. A., & Touchette, B. W. (2007). Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology, 350, 46-72. [ Links ]
CARICOMP. (2001). CARICOMP methods manual levels 1 and 2: manual of methods for mapping and monitoring of physical and biological parameters in the coastal zone of the caribbean.CARICOMP Data Management Center Centre for Marine Sciences University of the West Indies Mona, Kingston, Jamaica, 91. [ Links ]
Carruthers, T. J. B., Barnes, P. A. G., Jacome, G. E., & Fourqurean, J. W. (2005). Lagoon scale processes in a coastally influenced Caribbean system: implications for the seagrass Thalassia testudinum. Caribbean Journal of Science, 41(3), 441-455. [ Links ]
Casares, F. A. & Creed, J. C. (2008). Do small seagrasses enhance density, richness and biodiversity of macrofauna? Journal of Coastal Research, 24(3), 790-797. [ Links ]
Cortés, J., Fonseca, A. C., Nivia-Ruiz, J., Nielsen-Muñoz, V., Samper-Villarreal, J., & Salas, E. (2010). Monitoring coral reefs, seagrasses and mangroves in Costa Rica (CARICOMP). Revista de Biología Tropical, 58(3), 1-22. [ Links ]
Cramer, K. L., Jackson, J. B. C., Angioletti, C. V., Leonard-Pingel, J., & Guilderson, T. P. (2012). Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching. Ecology Letters, 1-7. doi:10.1111/j.1461-0248.2012.01768.x. [ Links ]
Creed, J. C., Phillips, R. C., & Tussenbroek, B. I. Van. (2003). The seagrasses of the Caribbean. In E. P. Green & F. T. Short (Eds.), World Atlas of Seagrasses (pp. 234-242). Cambridge: UNEP-WCMC. [ Links ]
Cuevas, E., Liceaga-Correa, M., & Garduño-Andrade, M. (2007). Spatial characterization of a foraging area for immature hawksbill turtles (Eretmochelys imbricata) in Yucatan, Mexico. Amphibia-Reptilia, 28, 337-346. [ Links ]
D’Croz, L., del Rosario, J. B., & Góndola, P. (2005). The effect of fresh water runoff on the distribution of dissolved inorganic nutrients and plankton in the Bocas del Toro Archipelago, Caribbean Panama. Caribbean Journal of Science, 41(3), 414-429. [ Links ]
Duarte, C. M. (2002). The future of seagrass meadows. Environmental Conservation, 29(2), 192-206. [ Links ]
Duarte, C. M., & Chiscano, C. L. (1999). Seagrass biomass and production: a reassessment. Aquatic Botany, 65, 159-174. [ Links ]
Duarte, C. M., Marbà, N., Gacia, E., Fourqurean, J. W., Beggins, J., & Barrón, C. (2010). Seagrass community metabolism: assessing the carbon sink capacity of seagrass meadows. Global Biogeochemical Cycles, 24(GB4032), 1-8. [ Links ]
Enríquez, S., & Pantoja-Reyes, N. I. (2005). Form-function analysis of the effect of canopy morphology on leaf self-shading in the seagrass Thalassia testudinum. Oecologia, 145, 235-243. [ Links ]
Erftemeijer, P. L. A., & Robin-Lewis III, R. R. (2006). Environmental impacts of dredging on seagrasses: a review. Marine Pollution Bulletin, 52, 1553-1572. [ Links ]
Fonseca, A. C., Nielsen, V., & Cortés, J. (2007). Monitoreo de pastos marinos en Perezoso, Cahuita, Costa Rica (sitio CARICOMP). Revista de Biología Tropical, 55(1), 55-66. [ Links ]
Fourqurean, J. W., Powell, G. V. N., Kenworthy, W. J., & Zieman, J. C. (1995). The effects of long term manipulation of nutrient supply on competition between the seagrasses Thalassia testudinum and Halodule wrightii in Florida Bay. Oikos, 72(3), 349-358. [ Links ]
Fulweiler, R. W., Rabalais, N. N., & Heiskanen, A. S. (2012). The eutrophication commandments. Marine Pollution Bulletin, 64, 1997-1999. [ Links ]
Gacia, E., Littler, M. M., & Littler, D. S. (1999). An experimental test of the capacity of food web interactions (fish-epiphytes-seagrasses) to offset the negative consequences of eutrophication on seagrass communities. Estuarine, Coastal and Shelf Science, 48, 757-766. [ Links ]
Gardner, T. A., Côte, I. M., Gill, J. A., Grant, A., & Watkinson, A. R. (2003). Long-term region-wide declines in Caribbean corals. Science, 301, 958-960. [ Links ]
Green, E. P., & Short, F. T. (2003). World Atlas of Seagrasses. Berkley: University of California Press. [ Links ]
Green, S. O., & Webber, D. F. (2003). The effects of varying levels of eutrophication on phytoplankton and seagrass (Thalassia testudinum) populations of the southeast coast of Jamaica. Bulletin of Marine Science, 73(2), 443-456. [ Links ]
Guzmán, H. M., & Guevara, C. A. (1998). Arrecifes coralinos de Bocas del Toro, Panamá: I. Distribución, estructura y estado de conservación de los arrecifes continentales de la Laguna de Chiriquí y la Bahía Almirante. Revista de Biología Tropical, 46, 601-622. [ Links ]
Guzman, H. M. (2003). Caribbean coral reefs of Panama: present status and future perspectives. In J. Cortés (Ed.), Latin American Coral Reefs (pp. 241-274). Amsterdam: Elsevier. [ Links ]
Guzmán, H. M., Barnes, P. A. G., Lovelock, C. E., & Feller, I. C. (2005). A site description of the CARICOMP mangrove, seagrass and coral reef sites in Bocas del Toro, Panama. Caribbean Journal of Science, 41(3), 430-440. [ Links ]
Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F., & D’Agrosa, C. (2008). A global map of human impact on marine ecosystems. Science, 319, 948-952. [ Links ]
Harborne, A. R., Mumby, P. J., Micheli, F., Perry, C. T., Dahlgren, C. P., & Holmes, K. E. (2006). The functional value of Caribbean coral reef, seagrass and mangrove habitats to ecosystem processes. Advances in Marine Biology, 50, 57-189. [ Links ]
Heck, K. L., Jr., Hays, G., & Orth, R. J. (2003). Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series, 253, 123-136. [ Links ]
Holmer, M., Wirachwong, P., & Thomsen, M. S. (2011). Negative effects of stress-resistant drift algae and high temperature on a small ephemeral seagrass species. Marine Biology, 158, 297-309. [ Links ]
Juman, R. A. (2005). The structure and productivity of the Thalassia testudinum community in Bon Accord Lagoon, Tobago. Revista de Biología Tropical, 53(1), 219-227. [ Links ]
Kaufmann, K. W., & Thompson, R. C. (2005). Water temperature variation and the meteorological and hydrographic environment of Bocas del Toro, Panama. Caribbean Journal of Science, 41(3), 392-413. [ Links ]
Kennedy, H., Beggins, J., Duarte, C. M., Fourqurean, J. W., Holmer, M., & Marbà, N. (2010). Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochemical Cycles, 24,1-8. doi:10.1029/2010GB003848. [ Links ]
Krupp, L. S., Cortés, J., & Wolff, M. (2009). Growth dynamics and state of the seagrass Thalassia testudinum in the Gandoca-Manzanillo National Wildlife Refuge, Caribbean, Costa Rica. Revista de Biología Tropical, 57(Supl. 1), 187-201. [ Links ]
Lee, K. S., Park, S. R., & Kim, Y. K. (2007). Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. Journal of Experimental Marine Biology and Ecology, 350, 144-175. [ Links ]
Lewis, J. B. (1984). The Acropora inheritance: a reinterpretation of the development of fringing reefs in Barbados, West Indies. Coral Reefs, 3, 117-122. [ Links ]
Linton, D., & Fisher, T. (2004). CARICOMP Caribbean Coastal Marine Productivity Program 1993-2003. Kingston, Jamaica: Cent. Mar. Sci., Univ. West Indies. [ Links ]
Mumby, P. J., Edwards, A. J., Arias-González, E., Lindeman, K. C., Blackwell, P. G., & Gall, A. (2004). Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature, 427, 533-536. [ Links ]
Murdoch, T. J. T., Glasspool, A. F., Outerbridge, M., Ward, J., Manuel, S., & Gray, J. (2007). Large-scale decline in offshore seagrass meadows in Bermuda. Marine Ecology Progress Series, 339, 123-130. [ Links ]
Nagelkerken, I., Roberts, C. M., Van der Velde, G., Dorenbosch, M., Van Riel, M. C., & Cocheret de la Morinière, E. (2002). How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale. Marine Ecology Progress Series, 244, 299-305. [ Links ]
Nagelkerken, I., & Van der Velde, G. (2004). Relative importance of interlinked mangroves and seagrass beds as feeding habitats for juvenile reef fish on a Caribbean island. Marine Ecology Progress Series, 274, 153-159. [ Links ]
Nellemann, C., Corcoran, E., Duarte, C. M., Valdés, L., de Young, C., & Fonseca, L. (2009). Blue Carbon: a rapid response assessment. United Nations Environment Programme: Grid-Arendal. [ Links ]
Ogden, J. C. (2010). Marine spatial planning (MSP): a first step to ecosystem-based management (EBM) in the Wider Caribbean. Revista de Biología Tropical, 58(3), 71-79. [ Links ]
Orth, R. J., Carruthers, T. J., Dennison, W. C., Duarte, C. M., Fourqurean, J. W., & Heck, K. L. (2006). A global crisis for seagrass ecosystems. Bioscience, 56(12), 987-996. [ Links ]
Pandolfi, J. M., Bradbury, R. H., Sala, E., Hughes, T. P., Bjorndal, K. A., & Cooke, R. G. (2003). Global trajectories of the long-term decline of coral reef ecosystems. Science, 301, 955-958. [ Links ]
Rodríguez-Martínez, R. E., Ruíz-Rentería, F., Van Tussenbroek, B. I., Barba-Santos, G., Escalante-Mancera, E., & Jordán-Garza, G. (2010). Environmental state and tendencies of the Puerto Morelos CARICOMP site, Mexico. Revista de Biología Tropical, 58(3), 23-43. [ Links ]
Rodríguez-Ramírez, A., Garzón-Ferreira, J., Batista-Morales, A., Gil, D. L., Gómez-López, D. I., & Gómez-Campo, K. (2010). Temporal patterns in coral reef, seagrass and mangrove communities from Chengue bay CARICOMP site (Colombia): 1993-2008. Revista de Biología Tropical, 58(3), 45-62. [ Links ]
Russell, B. D., Connell, S. D., Uthicke, S., Muehllehner, N., Fabricius, K. E., & Hall-Spencer, J. M. (2013). Future seagrass beds: Can increased productivity lead to increased carbon storage? Marine Pollution Bulletin, in press. [ Links ]
Short, F. T., & Burdick, D. M. (1996). Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts. Estuaries, 19(3), 730-739. [ Links ]
Short, F. T., & Neckles, H. A. (1999). The effects of global climate change on seagrasses. Aquatic Botany, 63, 169-196. [ Links ]
Short, F. T., Polidoro, B., Livingstone, S. R., Carpenter, K. E., Bandeira, S. B., & Japar, S. (2011). Extinction risk assessment of the world’s seagrass species. Biological Conservation, 144, 1961-1971. [ Links ]
Tibbetts, J. (2006). Louisiana’s Wetlands: a lesson in nature appreciation. Environmental Health Perspectives, 114(1), A40-A43. [ Links ]
Tomasko, D. A., & Lapointe, B. E. (1991). Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Marine Ecology Progress Series, 35, 91-98. [ Links ]
Trombulak, S. E. (2006). Ley y Desorden: La participación, la política, y la planificación en el Archipiélago de Bocas del Toro (Vol. Paper 314). Available online digitalcollections.sit.edu/isp_collection/314. [ Links ]
Van Tussenbroek, B. I., Vonk, J. A., Stapel, J., Erftemeijer, P. L. A., Middelburg, J. J., & Zieman, J. C. (2006). The biology of Thalassia: paradigms and recent advances in research. In A. W. D. Larkum, R. J. Orth & C. M. Duarte (Eds.), Seagrasses: Biology, Ecology and Conservation (pp. 409-439). Netherlands: Springer. [ Links ]
Van Tussenbroek, B. I. (2011). Dynamics of seagrasses and associated algae in coral reef lagoons. Hidrobiologica, 21, 293-310. [ Links ]
Van-Tussenbroek, B. I., Smith, S. R., Absten, M., Gerace, D. T., Alcolado, P., & Gayle, P. M. H. (in press). CARICOMP seagrass monitoring: stability and change of seagrass communities throughout the Greater Caribbean. [ Links ]
Verweij, M. C., Nagelkerken, I., De Graaff, D., Peeters, M., Bakker, E. J., & Van der Velde, G. (2006). Structure, food and shade attract juvenile coral reef fish to mangrove and seagrass habitats: a field experiment. Marine Ecology Progress Series, 306, 257-268. [ Links ]
Wabnitz, C. C., Andréfouët, S., Torres-Pulliza, D., Müller-Karger, F. E., & Kramer, P. A. (2008). Regional-scale seagrass habitat mapping in the Wider Caribbean region using Landsat sensors: applications to conservation and ecology. Remote Sensing of Environment, 112,3455-3467. [ Links ]
Watson, D. J. (1947). Comparative physiological studies on the growth of field crops: I. Variations in net assimilation rate and leaf area between species and varieties and within and between years. Annals of Botany N.S., 11, 41-76. [ Links ]
Waycott, M., Duarte, C. M., Carruthers, T. J. B., Orth, R. J., Dennison, W. C., & Olyarnik, S. (2009). Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences, 106(30), 12377-12381. [ Links ]
Wear, D. J., Sullivan, M. J., Moore, A. D., & Millie, D. F. (1999). Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Marine Ecology Progress Series, 179, 201-213. [ Links ]
*Correspondencia a: 1Jorge M. López-Calderón: Programa de Botánica Marina, Departamento de Biología Marina, Universidad Autónoma de Baja California Sur, Apdo. Postal 19-B, La Paz, Baja California Sur, 23080, México; jlopez@uabcs.mx 2Héctor M. Guzmán: Smithsonian Tropical Research Institute, Box 0843-03092, Panama, Republic of Panama; guzmanh@si.edu 2Gabriel E. Jácome: Smithsonian Tropical Research Institute, Box 0843-03092, Panama, Republic of Panama; jacomeg@si.edu 3Penélope A. G. Barnes: Bermuda Institute of Ocean Sciences, 17 Biological Station, St. George’s, GE 01, Bermuda; pbarnes3@telus.net
Received 22-I-2013. Corrected 30-IV-2013. Accepted 31-V-2013.