Palabras clave
trophic ecology
Bayesian mixing models
sea urchins
Puerto Rico.
Isótopos estables
ecología trófica
modelos de mezcla
erizos de mar
Puerto Rico.
Cómo citar
Resumen
Las especies Echinometra lucunter, Echinometra viridis, Lytechinus variegatus, Tripneustes ventricosus, and Diadema antillarum son los erizos de mar más comunes en los hábitat litorales del Caribe. Los erizos de mar T. ventricosus y L. variegatus habitan generalmente los pastos marinos mientras que las otras tres especies se encuentran asociadas a sustratos rocosos. Los hábitos alimentarios de estas especies han sido bien documentados y son reconocidas como herbívoros – omnívoros; sin embargo, pocas de estas especies han sido caracterizadas isotópicamente. Utilizamos los isotopos estables para caracterizar estas cinco especies de erizos y establecer las posiciones tróficas para las especies que cohabitan los mismos ecosistemas. También cuantificamos la contribución de los recursos alimentarios para E. lucunter. Los erizos T. ventricosus y D. antillarum mostraron los mayores valores de δ15N y valores similares de δ13C que variaron desde -11.6 ± 0.63 a -10.4 ± 0.99 %; donde el erizo E. lucunter mostró los valores más negativos con -15.40 ± 0.76 %. Las comunidades de algas no mostraron diferencias en valores promedio de δ15N (F= 1.300, df= 3, p= 0.301), pero sí mostraron variaciones en los valores de δ13C (F= 7.410, df= 3, p= 0.001). Los estudios de amplitud de elipses de nicho determinaron que las especies de los biotopos rocosos (D. antillarum, E. lucunter y E. viridis) no mostraron solapamiento de nicho. Similar resultado también se encontró en las especies de erizos que habitan en los pastos marinos. Sin embargo, la distancia entre estas dos especies fue menor respecto a la distancia entre las especies de erizos que habitan en los sustratos rocosos. Nuestros resultados muestran que las especies que habitan en los pastos marinos mostraron valores más elevados de δ13C en comparación con las especies de los sustratos rocosos. No se encontraron diferencias espaciales para E. lucunter en δ15N, pero sí en δ13C. Los modelos de mezcla bayesianos demuestran la plasticidad alimentaria de E. lucunter, especie capaz de utilizar múltiples recursos algales dependiendo de la disponibilidad por sitio. Semejanzas en δ15N entre D. antillarum y T. ventricosus parecen indicar similitudes tróficas entre ambas especies. Si bien T. ventricosus es reconocido como omnívoro, D. antillarum siempre ha sido considerado un herbívoro generalista. Finalmente, la falta de solapamiento entre las especies en los dos biotopos parece indicar una estrategia de partición de recursos para evitar la competencia de nicho entre especies concurrentes.
Citas
Barrios, J., & Reyes, J. (2009). Hábitos alimenticios de Tripneustes ventricosus (Lamarck 1816) (Echinodermata, Echinoidea) en isla la Tortuga, Venezuela. Recursos Marinos Acuíferos, 2, 583-589.
Ben-David, M., & Schell, D. M. (2001). Mixing models in analyses of diet using multiple stable isotopes: a response. Oecologia, 127, 180-184.
Boecklen, W. J., Yarnes, C. T., Cook, B. A., & James, A. C. (2011). On the use of stable isotopes in trophic ecology. Annual Review in Ecology and Systematics, 42, 411-440.
Box, G. E. P., & Cox, D. R. (1964). An analysis of transformations (with discussion). Journal of the Royal Statistical Society B., 26, 211-252.
Bunn, S. E., Loneragan, N. R., & Kempster, M. A. (1995). Effects of Acid Washing on Stable Isotope Ratios of C and N in Penaeid Shrimp and Seagrass: Implications for Food-Web Studies Using Multiple Stable Isotopes. Limnology and Oceanography, 40(3), 622-625.
Cabanillas-Terán, N. (2009). Ecología y estatus trófico del erizo de mar Diadema antillarum (Philippi, 1845) en los fondos rocosos de las Islas Canarias (Gran Canaria, España). (Tesis doctoral). Universidad de las Palmas de Gran Canaria, España.
Caraveo-Patiño, J., & Soto, L. (2005). Stable carbon isotope ratios for the gray whale (Eschrichtius robustus) in the breeding grounds of Baja California Sur, México. Hydrobiologia, 539, 99-107.
Clark, J. J., & Wilcock, P. R. (2000). Effects of land-use change on channel morphology in northeastern Puerto Rico. GSA Bulletin, 112(12), 15.
Cloern, J. E. (2001). Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series, 210, 223-253.
Caut, S., Angulo, E., & Courchamp, F. (2008). Discrimination factors (δ15N and δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Functional Ecology, 22, 255-263.
De Niro, M. J., & Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45, 341-351.
Fry, B., & Sherr, E. B. (1989). δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contribution to Marine Science, 27, 13-47.
Hawkins, C. M. (1981). Efficiency of organic matter absorption by the tropical echinoid Diadema antillarum Philippi fed non-macrophytic algae. Journal of Experimental Marine Biology and Ecology, 49(2), 245-253.
Hendler, G., Miller, J. E., Pawson, D. L., & Kier, P. M. (1995). Sea Stars, Sea Urchins, and Allies. Echinoderms of Florida and the Caribbean. Smithsonian Institution Press.
Hernández, J. C., Brito, A., García, N., Gil-Rodríguez, M. C., Herrera, G., Cruz-Reyes, A., & Falcón, J.M. (2006). Spatial and seasonal variation of the gonad index of Diadema antillarum (Echinodermata: Echinoidea) in the Canary Islands. Scientia Marina, 70(4), 689-698.
Herrera-López, G., Cruz-Reyes, A., Hernández, J. C., García, N., González-Lorenzo, G., Gil-Rodríguez, M. C., Brito, A., & Falcón, J. M. (2004). Alimentación y diversidad algal en la dieta del erizo Diadema antillarum en Tenerife. Revista Academia Canarias Ciencias, 15(3/4), 129-141.
Hobson, K. A., & Sease, J. L. (1998). Stable isotope analyses of tooth annuli reveal temporal dietary records: an example using Steller sea lions. Marine Mammal Science, 14, 116-129.
Jackson, A. L., Inger, R., Parnell, A. C., & Bearhop, S. (2011). Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology, 80(3), 595-602.
Karlson, R. H. (1983). Disturbance and monopolization of a spatial resource by Zoanthus sociatus (Coelenterata, Anthozoa). Bulletin of Marine Science, 33, 118-131.
Keller, B. D. (1983). Coexistence of sea urchins in seagrass meadows: an experimental analysis of competition and predation. Ecology, 64(6), 1581-1598.
Klinger, T. S., Hsieh, H. L., Pangallo, R. A., Chen, C. P., & Lawrence, J. M. (1986). The effect of temperature on feeding, digestion, and absorption of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea). Physiological Zoology, 59(3)332-336.
Lawrence, J. M., Lawrence, A. L., & Watts, S. A. (2013). Feeding, digestion, and digestibility of sea urchins. In J. M. Lawrence (Ed.), Sea Urchins, Biology and Ecology (Chapter 9, pp. 135-154). Amsterdam: Elsevier BV.
Lewis, J. B. (1964). Feeding and digestion in the tropical sea urchin Diadema antillarum Philippi. Canadian Journal of Zoology, 42(4), 549-557.
Littler, D. S., & Littler, M. M. (2000). Caribbean reef plants. Washington, DC: Offshore Graphics Inc.
Mahon, R., & Parker, C. (1999). Barbados sea eggs, past, present and future. Fisheries Division, Ministry of Agriculture and Rural Development, Barbados Fisheries Management Plan, Public Information Document.
McCutchan, J. H., Lewis, W. M., Kendall, C., & McGrath, C. C. (2003). Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos, 102, 378-390.
McGlathery, K. J. (2001). Macroalgal blooms contribute to the decline of seagrass in nutrient-enriched coastal waters. Journal of Phycology, 37, 453-56.
McPherson, B. F. (1969). Studies on the biology of the tropical sea urchins Echinometra lucunter and Echinometra viridis. Bulletin of Marine Science, 19, 194-213.
Minagawa, M., & Wada, E. (1984). Stepwise enrichment of 15N along food hains: further evidence and the relation between 15N and animal age. Geochimestry and Cosmochimestry Acta, 48, 1135-1140.
Nixon, S. W., Ammerman, J. W., Atkinson, L. P., Berounsky, V. M., Billen, G., Boicourt, W. C., & Seitzinger, S. P. (1996). The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry, 35, 141-180.
Parnell, A. C., Inger, R., Bearhop, S., & Jackson, A. L. (2010). Source Partitioning Using Stable Isotopes: Coping with Too Much Variation. PLOS one, 5(3), 1-5.
Parnell, A., & Jackson, A. (2013). Siar: Stable Isotope Analysis in R. R package version 4.2. Downloaded from http//CRAN.Rproject.org/package=siar
Peterson, B. J., & Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review in Ecology and Systematic, 18, 293-320.
Peterson, B. J., Howarth, R. W., & Garritt, R. H. (1985). Multiple stable isotopes used to trace the flow of organic matter flow in estuarine food webs. Science, 227, 1361-1363.
Pinnegar, J. K., & Polunin, N. V. C. (2000). Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia, 122(3), 399-409.
Phillips, D. (2012). Converting isotope values to diet composition: the use of mixing models. Journal of Mammalogy, 93(2), 342-352.
Post, D. M. (2002). Using stable isotopes to estimate trophic position models, methods, and assumptions. Ecology, 83(3), 703-718.
Prado, P. P., Alcoverro, T., & Romero, J. (2010). Influence of nutrients in the feeding ecology of seagrass (Posidonia oceanica L.) consumers: a stable isotopes approach. Marine Biology, 157, 715-724.
Prado, P., Carmichael, R. H., Watts, S. A., Cebria, J., & Heck, Jr. K. L. (2012). Diet-dependent δ13C and δ15N fractionation among sea urchin Lytechinus variegatus tissues: implications for food web models. Marine Ecology Progress Series, 462, 175.
R Development Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0. http://www.R-project.org/
Rezende, C. E., Lacerda, L. D., Ovall, A. R. C., Silva, C. A. R., & Martinelli, L. A. (1990). Nature of POC transport in a mangrove ecosystem: a carbon stable isotopic study. Estuarine, Coastal and Shelf Science, 30(6), 641-645.
Rodríguez, S. R. (2003). Consumption of drift kelp by intertidal populations of the sea urchin Tetrapygus niger on the central Chilean coast: possible consequences at different ecological levels. Marine Ecology Progress Series, 251, 141-151.
Rodríguez-Barreras, R., Cuevas, E., Cabanillas-Terán, N., & Sabat, A. M. (2015). Potential omnivory of the sea urchin Diadema antillarum? Regional Studies in Marine Science, 2, 11-18.
Rodríguez-Barreras, R., Pérez, M. E., Williams, S. M., Mercado-Molina, A. E., & Sabat, A. M. (2014). Higher population densities of the sea urchin Diadema antillarum linked to wave sheltered areas in north Puerto Rico Archipelago. Journal of the Marine Biological Association of the U.K., 94(8), 1661-1669.
Rotjan, R. D., & Lewis, S. M. (2008). Impact of coral predators on tropical reefs. Marine Ecology Progress Series, 367, 73-91.
Semmens, B. X., Moore, J. W., & Ward, E. J. (2009). Improving Bayesian isotope mixing models: a response to. Ecology Letters, 12, E6-E8.
Serafy, D. K. (1979). Echinoids (Echinodermata: Echinoidea). Memoirs of the Hourglass Cruises, 5, 120.
Solomon, C. T., Carpenter, S. R., Clayton, M. K., Cole, J. J., Coloso, J. J., Pace, M. L., Vander Zanden, M. K., & Weidel, B. C. (2011). Terrestrial, benthic, and pelagic resource use in lakes: results from a three-isotope Bayesian mixing model. Ecology, 92, 1115-1125.
Szepanski, M. M., Ben-David, M., & Van Ballenberghe, V. (1999). Assessment of anadromous salmon resources in the diet of the Alexander Archipelago wolf using stable isotope analysis. Oecologia, 120, 327-335.
Tertschnig, W. P. (1989). Diel activity patterns and foraging dynamics of the sea urchin Tripneustes ventricosus in a tropical seagrass community and a reef environment (Virgin Islands). Marine Ecology, 10, 3-21.
Tewfik, A., Rasmussen, J., & McCann, K. S. (2005). Anthropogenic enrichment alters a marine benthic food web. Ecology, 86(10), 2726-2736.
Tomas, F., Alvarez-Cascos, D., Turon, X., & Romero, J. (2006). Differential element assimilation by sea grass urchin Paracentrotus lividus in seagrass beds: implications for trophic interactions. Marine Ecology Progress Series, 306, 125-131.
Trenzado, C. E., Hidalgo, F., Villanueva, D., Furné, M., Díaz-Casado, M. E., Merino, R., & Sanz, A. (2012). Study of the enzymatic digestive profile in three species of Mediterranean sea urchins. Aquaculture, 344, 174-180.
U. S. G. S. (1996). Atlas of ground-water resources in Puerto Rico and the U.S. Virgin Islands. T. D. Veve and B. E. Taggart (Eds.). Water resources investigation report (94-4198, 151 p.).
Van-Dover, C. L., Grassle, J. F., Fry, B., Garrit, R. H., & Starczak, V. R. (1992). Stable isotopes evidence for entry of sewage-derived organic material into a deep-sea food web. Organic Geochemistry, 27, 103-113.
Vander-Zanden, M. J., & Rasmussen, J. B. (2001). Variation in δ15Ν and δ13 C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography, 46(8), 2061-2066.
Vanderklift, M. A., & Ponsard, S. (2003). Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia, 136, 169-182.
Vanderklift, M. A., Kendrick, G. A., & Smith, A. J. (2006). Differences in trophic position among sympatric sea urchin species. Estuarine, Coastal and Shelf Science, 66, 291-297.
Villinski, J. C., Hayes, J. M., Villinski, J. T., Brassell, S. C., & Raff, R. A. (2004). Carbon-isotopic shifts associated with heterotrophy and biosynthetic pathways in direct and indirect-developing sea urchins. Marine Ecology Progress Series, 275, 139-151.
Wangensteen, O. S., Turón, X., García-Cisneros, A., Recasens, M., Romero, J., & Palacín, C. (2011). A wolf in sheep’s clothing: carnivory in dominant sea urchins in the Mediterranean. Marine Ecology Progress Series, 441, 117-128.
Wing, S. R., McLeod, R. J., Clark, K. L., & Frew, R. D. (2008). Plasticity in the diet of two echinoderm species across an ecotone: microbial recycling of forest litter and bottom-up forcing of populations structure. Marine Pollution Bulletin, 360, 115-123.
Wolf, N., Scott, A., & Martínez del Río, C. (2009). Nutritional ecology: Ten years of experimental animal isotopic ecology. Functional Ecology, 23, 17-26.
Zar, J. H. (2010). Biostatistical analysis (5th Edition). Upper Saddle River, Prentice Hall, Upper Saddle River, New Jersey.
Zieman, J. C., Macko, S. A., & Mills, A. L. (1984). Role of seagrasses and mangroves in estuarine food webs: temporal and spatial changes in stable isotope composition and amino acid content during decomposition. Bulletin of Marine Science, 35(3), 380-392.
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