Spatial and temporal variation of the δ15N in Thalassia testudinum in the Mexican Caribbean (2009–2017)
Alberto Sánchez A C , Dilian Anguas-Cabrera A , Karla Camacho-Cruz A B , M. Concepción Ortiz-Hernández B and Sergio Aguíñiga-García AA Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Avenida IPN S/N, Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur, CP 23096, México.
B El Colegio de la Frontera Sur (ECOSUR), Unidad Chetumal, Avenida Centenario kilómetro 5.5, C.P.77014, Chetumal, Quintana Roo, México.
C Corresponding author. Email: alsanchezg@ipn.mx; alsanchezg13@gmail.com
Marine and Freshwater Research 71(8) 905-912 https://doi.org/10.1071/MF19105
Submitted: 23 March 2019 Accepted: 23 January 2020 Published: 17 March 2020
Abstract
Wastewater pollution in seagrass has been documented for decades. In areas where baseline data are lacking, such as the Mexican Caribbean, the δ15N of seagrass can provide information on status and trends. The aims of this study were to determine the spatial and temporal variation in δ15N values of T. testudinum from 2009 to 2017, to explore the nature and causes of isotopic variability, which must be fully understood, and to examine how isotopic variability is linked to wastewater on the coast. Samples of T. testudinum were collected during 2011–2017 in Cancún and from 2009 to 2017 in Mahahual, and analysed on a mass spectrometer. The δ15N values in Cancún (9.0 ± 1.3 ‰) were significantly (P < 0.005) higher than those in Mahahual (1.9 ± 0.9 ‰). Our results reflect the continuous supply of wastewater as a source of 15N in Cancún and the atmospheric deposition of dissolved inorganic nitrogen from uncontaminated groundwater in Mahahual. Mahahual is an ideal site to continue environmental monitoring of the healthy seagrass in the southern Mexican Caribbean. Meanwhile, measures on the treatment and final disposal of wastewater in Cancun must be addressed with a great priority.
Additional keywords: Caribbean Sea, karstic spring, nitrogen isotopes, water quality.
References
Ayala-Mejía, M. G. (1993). Estudio de la calidad del agua del sistema lagunar Nichupté en Cancún, Quintana Roo. BSc thesis, Universidad Autónoma Metropolitana, Unidad Iztapalapa, Ciudad de México México.Baker, D. M., MacAvoy, S. E., and Kim, K. (2007). Relationship between water quality, δ15N, and aspergillosis of Caribbean Sea fan corals. Marine Ecology Progress Series 343, 123–130.
| Relationship between water quality, δ15N, and aspergillosis of Caribbean Sea fan corals.Crossref | GoogleScholarGoogle Scholar |
Baker, D. M., Jordán-Dahlgren, E., Maldonado, M. A., and Harvell, C. D. (2010). Sea fan corals provide a stable isotope baseline for assessing sewage pollution in the Mexican Caribbean. Limnology and Oceanography 55, 2139–2149.
| Sea fan corals provide a stable isotope baseline for assessing sewage pollution in the Mexican Caribbean.Crossref | GoogleScholarGoogle Scholar |
Baker, D. M., Rodriguez-Martinez, R. E., and Fogel, M. L. (2013). Tourism’s nitrogen footprint on a Mesoamerican coral reef. Coral Reefs 32, 691–699.
| Tourism’s nitrogen footprint on a Mesoamerican coral reef.Crossref | GoogleScholarGoogle Scholar |
Baker, D. M., Murdoch, T. J., Conti-Jerpe, I., and Fogel, M. (2017). Investigating Bermuda’s pollution history through stable isotope analyses of modern and museum-held gorgonian corals. Marine Pollution Bulletin 114, 169–175.
| Investigating Bermuda’s pollution history through stable isotope analyses of modern and museum-held gorgonian corals.Crossref | GoogleScholarGoogle Scholar | 27600272PubMed |
Barlow, P. (2003). Ground water in fresh–saltwater environments of the Atlantic Coast. Circular 1262, US Geological Survey, Washington, DC, USA.
Bowen, J. L., Kroeger, K. D., Tomasky, G., Pabich, W. J., Cole, M. L., Carmichael, R. H., and Valiela, I. (2007). A review of land–sea coupling by groundwater discharge of nitrogen to New England estuaries: mechanisms and effects. Applied Geochemistry 22, 175–191.
| A review of land–sea coupling by groundwater discharge of nitrogen to New England estuaries: mechanisms and effects.Crossref | GoogleScholarGoogle Scholar |
Bratton, J. F., Böhlke, J. K., Manheim, F. M., and Krantz, D. E. (2004). Submarine ground water in Delmarva Peninsula coastal bays: ages and nutrients. Ground Water 42, 1021–1034.
| Submarine ground water in Delmarva Peninsula coastal bays: ages and nutrients.Crossref | GoogleScholarGoogle Scholar |
Camacho-Cruz, K. A., Ortiz-Hernández, M. C., Sánchez, A., Carrillo, L., and Navarrete, A. D. J. (2019). Water quality in the eastern karst region of the Yucatan Peninsula: nutrients and stable nitrogen isotopes in turtle grass, Thalassia testudinum. Environmental Science and Pollution Research International , .
| Water quality in the eastern karst region of the Yucatan Peninsula: nutrients and stable nitrogen isotopes in turtle grass, Thalassia testudinum.Crossref | GoogleScholarGoogle Scholar | 30903477PubMed |
Campbell, J. E., and Fourqurean, J. W. (2009). Interspecific variation in the elemental and stable isotope content of seagrasses in South Florida. Marine Ecology Progress Series 387, 109–123.
| Interspecific variation in the elemental and stable isotope content of seagrasses in South Florida.Crossref | GoogleScholarGoogle Scholar |
Campbell, J. E., and Fourqurean, J. W. (2018). Does nutrient availability regulate seagrass response to elevated CO2? Ecosystems 21, 1269–1282.
| Does nutrient availability regulate seagrass response to elevated CO2?Crossref | GoogleScholarGoogle Scholar |
Carbajal-Pérez, N. (2009). ‘Hidrodinámica y Transporte de Contaminantes y Sedimentos en el Sistema Lagunar de Nichupté–Bojórquez, Quintana Roo.’ Informe final SNIB-CONABIO proyecto no. CQ063. (Instituto Potosino de Investigación Científica y Tecnológica: A.C. México, D.F., México.)
Carrillo, L., Johns, E. M., Smith, R. H., Lamkin, J. T., and Largier, J. L. (2016). Pathways and hydrography in the Mesoamerican Barrier Reef System. Part 2: water masses and thermohaline structure. Continental Shelf Research 120, 41–58.
| Pathways and hydrography in the Mesoamerican Barrier Reef System. Part 2: water masses and thermohaline structure.Crossref | GoogleScholarGoogle Scholar |
Carruthers, T. J. B., van Tussenbroek, B. I., and Dennison, W. C. (2005). Influence of submarine springs and wastewater on nutrient dynamics of Caribbean seagrass meadows. Estuarine, Coastal and Shelf Science 64, 191–199.
| Influence of submarine springs and wastewater on nutrient dynamics of Caribbean seagrass meadows.Crossref | GoogleScholarGoogle Scholar |
Coronado, C., Candela, J., Iglesias-Prieto, R., Sheinbaum, J., López, M., and Ocampo-Torres, F. J. (2007). On the circulation in the Puerto Morelos fringing reef lagoon. Coral Reefs 26, 149–163.
| On the circulation in the Puerto Morelos fringing reef lagoon.Crossref | GoogleScholarGoogle Scholar |
Cruz-Toledo, J. C. (2011). Influencia de las actividades antropogénicas en ecosistemas costeros carbonatados de Quintana Roo. México. MSc thesis, Universidad Autónoma Metropolitana, Unidad Iztapalapa, Ciudad de México, México.
Culhuac-Schmidt, S. E. (1987). Importancia ecológica de las algas epifitas de las fanerógamas marinas en la Laguna Bojórquez, Quintana Roo. BSc thesis, Universidad Autónoma Metropolitana, Unidad Iztapalapa, Ciudad de México, México.
Duarte, C. M. (1990). Seagrass nutrient content. Marine Ecology Progress Series 67, 201–207.
| Seagrass nutrient content.Crossref | GoogleScholarGoogle Scholar |
Fogel, M. L., and Paerl, H. W. (1993). Isotopic tracers of nitrogen from atmospheric deposition to coastal waters. Chemical Geology 107, 233–236.
| Isotopic tracers of nitrogen from atmospheric deposition to coastal waters.Crossref | GoogleScholarGoogle Scholar |
Fourqurean, J. W., Escorcia, S. P., Anderson, W. T., and Zieman, J. C. (2005). Spatial and seasonal variability in elemental content, δ13C, and δ15N of Thalassia testudinum from south Florida and its implications for ecosystem studies. Estuaries 28, 447–461.
| Spatial and seasonal variability in elemental content, δ13C, and δ15N of Thalassia testudinum from south Florida and its implications for ecosystem studies.Crossref | GoogleScholarGoogle Scholar |
Fourqurean, J. W., Manuel, S. A., Coates, K. A., Kenworthy, W. J., and Boyer, J. N. (2015). Water quality, isoscapes and stoichioscapes of seagrasses indicate general P limitation and unique N cycling in shallow water benthos of Bermuda. Biogeosciences 12, 6235–6249.
| Water quality, isoscapes and stoichioscapes of seagrasses indicate general P limitation and unique N cycling in shallow water benthos of Bermuda.Crossref | GoogleScholarGoogle Scholar |
Gallegos, M. E., Merino, M., Marba, N., and Duarte, C. M. (1993). Biomass and dynamics of Thalassia testudinum in the Mexican Caribbean: elucidating rhizome growth. Marine Ecology Progress Series 95, 185–192.
| Biomass and dynamics of Thalassia testudinum in the Mexican Caribbean: elucidating rhizome growth.Crossref | GoogleScholarGoogle Scholar |
Gil, M. A., Renfro, B., Figueroa-Zavala, B., Peiné, I., and Kenneth, H. D. (2015). Rapid tourism growth and declining coral reefs in Akumal, Mexico. Marine Biology , .
| Rapid tourism growth and declining coral reefs in Akumal, Mexico.Crossref | GoogleScholarGoogle Scholar |
Hernández-Terrones, L., Rebolledo-Vieyra, M., Merino-Ibarra, M., Soto, M., Le-Cossec, A., and Monroy-Ríos, E. (2011). Groundwater pollution in a karstic region (NE Yucatan): baseline nutrient content and flux to coastal ecosystems. Water, Air, and Soil Pollution 218, 517–528.
| Groundwater pollution in a karstic region (NE Yucatan): baseline nutrient content and flux to coastal ecosystems.Crossref | GoogleScholarGoogle Scholar |
Hernández-Terrones, L. M., Null, K. A., Ortega-Camacho, D., and Paytan, A. (2015). Water quality assessment in the Mexican Caribbean: impacts on the coastal ecosystem. Continental Shelf Research 102, 62–72.
| Water quality assessment in the Mexican Caribbean: impacts on the coastal ecosystem.Crossref | GoogleScholarGoogle Scholar |
Holon, F., Marre, G., Parravicini, V., Mouquet, N., Bockel, T., Descamp, P., Tribot, A. S., Boissery, P., and Deter, J. (2018). A predictive model based on multiple coastal anthropogenic pressures explains the degradation status of a marine ecosystem: implications for management and conservation. Biological Conservation 222, 125–135.
| A predictive model based on multiple coastal anthropogenic pressures explains the degradation status of a marine ecosystem: implications for management and conservation.Crossref | GoogleScholarGoogle Scholar |
INEGI (2017). Anuario de estadísticas por entidad federativa. Instituto Nacional de Estadística, Geografía, México. Available at: http://internet.contenidos.inegi.org.mx/contenidos/Productos/prod_serv/contenidos/espanol/bvinegi/productos/nueva_estruc/aegef_2017/702825097929.pdf
Jennerjahn, T. C. (2012). Biogeochemical response of tropical coastal systems to present and past environmental change. Earth-Science Reviews 114, 19–41.
| Biogeochemical response of tropical coastal systems to present and past environmental change.Crossref | GoogleScholarGoogle Scholar |
Lecher, A., and Mackey, K. (2018). Synthesizing the effects of submarine groundwater discharge on marine biota. Hydrology 5, 60.
| Synthesizing the effects of submarine groundwater discharge on marine biota.Crossref | GoogleScholarGoogle Scholar |
McCrackin, M. L., Cooter, E. J., Dennis, R. L., Harrison, J. A., and Compton, J. E. (2017). Alternative futures of dissolved inorganic nitrogen export from the Mississippi River Basin: influence of crop management, atmospheric deposition, and population growth. Biogeochemistry 133, 263–277.
| Alternative futures of dissolved inorganic nitrogen export from the Mississippi River Basin: influence of crop management, atmospheric deposition, and population growth.Crossref | GoogleScholarGoogle Scholar | 30505046PubMed |
Molina Hernández, A. L., and van Tussenbroek, B. I. (2014). Patch dynamics and species shifts in seagrass communities under moderate and high grazing pressure by green sea turtles. Marine Ecology Progress Series 517, 143–157.
| Patch dynamics and species shifts in seagrass communities under moderate and high grazing pressure by green sea turtles.Crossref | GoogleScholarGoogle Scholar |
Mutchler, T., and Hoffman, D. K. (2017). Response of seagrass (Thalassia testudinum) metrics to short-term nutrient enrichment and grazing manipulations. Journal of Experimental Marine Biology and Ecology 486, 105–113.
| Response of seagrass (Thalassia testudinum) metrics to short-term nutrient enrichment and grazing manipulations.Crossref | GoogleScholarGoogle Scholar |
Mutchler, T., Dunton, K. H., Townsend-Small, A., Fredriksen, S., and Rasser, M. K. (2007). Isotopic and elemental indicators for nutrient sources and status of coastal habitats in the Caribbean Sea, Yucatan Peninsula, Mexico. Estuarine, Coastal and Shelf Science 74, 449–457.
| Isotopic and elemental indicators for nutrient sources and status of coastal habitats in the Caribbean Sea, Yucatan Peninsula, Mexico.Crossref | GoogleScholarGoogle Scholar |
Mutchler, T., Mooney, R. F., Wallace, S., Podsim, L., Fredriksen, S., and Dunton, K. H. (2010). Origins and fate of inorganic-nitrogen from land to coastal ocean on the Yucatan Peninsula, Mexico. In ‘Coastal Lagoons Critical Habitats of Environmental Change’. (Eds M. J. Kennish and H. W. Paerl.) pp. 285–305. (CRC Press: Boca Raton, FL, USA.)
Null, K. A., Knee, L. K., Crook, E. D., de Sieyes, N. R., Rebolledo-Vieyra, M., Hernández-Terrones, L., and Paytan, A. (2014). Composition and fluxes of submarine groundwater along the Caribbean coast of the Yucatan Peninsula. Continental Shelf Research 77, 38–50.
| Composition and fluxes of submarine groundwater along the Caribbean coast of the Yucatan Peninsula.Crossref | GoogleScholarGoogle Scholar |
O’Brien, K. R., Waycott, M., Maxwell, P., Kendrick, G. A., Udy, J. W., Ferguson, A. J., Kilminster, K., Scanes, P., McKenzie, L. J., McMahon, K., Adams, M. P., Samper-Villareal, J., Collier, C., Lyons, M., Mumby, P. J., Radke, L., Christianen, M. J. A., and Dennison, W. C. (2018). Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance. Marine Pollution Bulletin 134, 166–176.
| Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance.Crossref | GoogleScholarGoogle Scholar | 28935363PubMed |
Olsen, Y. S., and Valiela, I. (2010). Effect of sediment nutrient enrichment and grazing on turtle grass Thalassia testudinum in Jobos Bay, Puerto Rico. Estuaries and Coasts 33, 769–783.
| Effect of sediment nutrient enrichment and grazing on turtle grass Thalassia testudinum in Jobos Bay, Puerto Rico.Crossref | GoogleScholarGoogle Scholar |
Orth, R. J., Carruthers, T. J. B., Dennison, W. C., Duarte, C. M., Fourqurean, J. W., Heck, K. L., Hughes, A. R., Kendrick, G. A., Kenworthy, W. J., Olyarnik, S., Short, F. T., Waycott, M., and Williams, S. L. (2006). A global crisis for seagrass ecosystems. Bioscience 56, 987–996.
| A global crisis for seagrass ecosystems.Crossref | GoogleScholarGoogle Scholar |
Parra, S. M., Valle-Levinson, A., Mariño-Tapia, I., and Enriquez, C. (2015). Salt intrusion at a submarine spring in a fringing reef lagoon. Journal of Geophysical Research. Oceans 120, 2736–2750.
| Salt intrusion at a submarine spring in a fringing reef lagoon.Crossref | GoogleScholarGoogle Scholar |
Parra, S. M., Valle-Levinson, A., Mariño-Tapia, I., Enriquez, C., Candela, J., and Sheinbaum, J. (2016). Seasonal variability of saltwater intrusion at a point-source submarine groundwater discharge. Limnology and Oceanography 61, 1245–1258.
| Seasonal variability of saltwater intrusion at a point-source submarine groundwater discharge.Crossref | GoogleScholarGoogle Scholar |
Piñón-Gimate, A., Espinosa-Andrade, N., Sánchez, A., and Casas-Valdez, M. (2017). Nitrogen isotopic characterization of macroalgae blooms from different sites within a subtropical bay in the Gulf of California. Marine Pollution Bulletin 116, 130–136.
| Nitrogen isotopic characterization of macroalgae blooms from different sites within a subtropical bay in the Gulf of California.Crossref | GoogleScholarGoogle Scholar | 28063698PubMed |
Risk, M., Lapointe, B., Sherwood, O., and Bedford, B. (2009). The use of δ15N in assessing sewage stress on coral reefs. Marine Pollution Bulletin 58, 793–802.
| The use of δ15N in assessing sewage stress on coral reefs.Crossref | GoogleScholarGoogle Scholar | 19286230PubMed |
Risk, M. J., Burchell, M., Brunton, D. A., and McCord, M. R. (2014). Health of the coral reefs at the US Navy Base, Guantánamo Bay, Cuba: a preliminary report based on isotopic records from gorgonians. Marine Pollution Bulletin 83, 282–289.
| Health of the coral reefs at the US Navy Base, Guantánamo Bay, Cuba: a preliminary report based on isotopic records from gorgonians.Crossref | GoogleScholarGoogle Scholar | 24735775PubMed |
Roca, G., Alcoverro, T., Krause-Jensen, D., Balsby, T. J. S., van Katwijk, M. M., Marbà, N., Santos, R., Arthur, R., Mascaró, O., Fernández-Torquemada, Y., Pérez, M., Duarte, C. M., and Romero, J. (2016). Response of seagrass indicators to shifts in environmental stressors: a global review and management synthesis. Ecological Indicators 63, 310–323.
| Response of seagrass indicators to shifts in environmental stressors: a global review and management synthesis.Crossref | GoogleScholarGoogle Scholar |
Romero-Sierra, P., Rivas, D., Almazán-Becerril, A., and Hernández-Terrones, L. (2018). Hydrochemistry and hydrodynamics of a Mexican Caribbean Lagoon: Nichupté lagoon system. Estuarine, Coastal and Shelf Science 215, 185–198.
| Hydrochemistry and hydrodynamics of a Mexican Caribbean Lagoon: Nichupté lagoon system.Crossref | GoogleScholarGoogle Scholar |
Rosiles-González, G., Ávila-Torres, G., Moreno-Valenzuela, O. A., Acosta-González, G., Leal-Bautista, R. M., Grimaldo-Hernández, C. D., Brown, J. K., Chaidez-Quiroz, C., Betancourt, W. Q., Gerba, C. P., and Hernández-Zepeda, C. (2017). Occurrence of pepper mild mottle virus (PMMoV) in groundwater from a karst aquifer system in the Yucatan Peninsula, Mexico. Food and Environmental Virology 9, 487–497.
| Occurrence of pepper mild mottle virus (PMMoV) in groundwater from a karst aquifer system in the Yucatan Peninsula, Mexico.Crossref | GoogleScholarGoogle Scholar | 28646449PubMed |
Saint-Loup, R., Felix, T., Maqueda, A., Schiller, A., and Renard, P. (2018). A survey of groundwater quality in Tulum region, Yucatan Peninsula, Mexico. Environmental Earth Sciences 77, 644.
| A survey of groundwater quality in Tulum region, Yucatan Peninsula, Mexico.Crossref | GoogleScholarGoogle Scholar |
Sánchez, A., Ortiz-Hernández, M. C., Talavera-Sáenz, A., and Aguíñiga-García, S. (2013). Stable nitrogen isotopes in the turtle grass Thalassia testudinum from the Mexican Caribbean: implications of anthropogenic development. Estuarine, Coastal and Shelf Science 135, 86–93.
| Stable nitrogen isotopes in the turtle grass Thalassia testudinum from the Mexican Caribbean: implications of anthropogenic development.Crossref | GoogleScholarGoogle Scholar |
SEDETUR (2018). Resultados de la actividad turística 2018. Secretaria de Turismo. Available at http://www.datatur.sectur.gob.mx/SitePages/versionesRAT.aspx
Sherwood, O. A., Lehmann, M. F., Schubert, C. J., Scott, D. B., and McCarthy, M. D. (2011). Nutrient regime shift in the western North Atlantic indicated by compound-specific δ15N of deep-sea gorgonian corals. Proceedings of the National Academy of Sciences of the United States of America 108, 1011–1015.
| Nutrient regime shift in the western North Atlantic indicated by compound-specific δ15N of deep-sea gorgonian corals.Crossref | GoogleScholarGoogle Scholar | 21199952PubMed |
Short, F. T., Short, C. A., and Novak, A. B. (2018). Seagrasses. In ‘The Wetland Book: II: Distribution, Description, and Conservation’. (Eds C. M. Finlayson, R. Milton, C. Prentice, and N. C. Davidson.) pp. 74–90. (Springer: Dordrecht, Netherlands.)
Sima-Morales, J. A. L. (2004). Hidrología y estado trófico de las lagunas costeras del caribe mexicano: aportes de nutrientes de diferentes fuentes. MSc thesis, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mérida, Yucatán, México.
van Tussenbroek, B. I. (1995). Thalassia testudinum leaf dynamics in a Mexican Caribbean coral reef lagoon. Marine Biology 122, 33–40.
| Thalassia testudinum leaf dynamics in a Mexican Caribbean coral reef lagoon.Crossref | GoogleScholarGoogle Scholar |
van Tussenbroek, B. I., Hermus, K., and Tahey, T. (1996). Thalassia testudinum (Banks ex Konig) biomass and growth in a shallow tropical lagoon system, in relation to tourist development. Caribbean Journal of Science 32, 357–364.
Ward-Paige, C. A., Risk, M. J., and Sherwood, O. A. (2005). Reconstruction of nitrogen sources on coral reefs: δ15N and δ13C in gorgonians from Florida Reef Tract. Marine Ecology Progress Series 296, 155–163.
| Reconstruction of nitrogen sources on coral reefs: δ15N and δ13C in gorgonians from Florida Reef Tract.Crossref | GoogleScholarGoogle Scholar |