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Tourism’s nitrogen footprint on a Mesoamerican coral reef

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Abstract

Globally, the eutrophication of coastal marine environments is a worsening problem that is accelerating the loss of biodiversity and ecosystem services. Coral reefs are among the most sensitive to this change, as chronic inputs of agricultural and wastewater effluents and atmospheric deposition disrupt their naturally oligotrophic state. Often, anthropogenic alteration of the coastal nitrogen pool can proceed undetected as rapid mixing with ocean waters can mask chronic and ephemeral nitrogen inputs. Monitoring nitrogen stable isotope values (δ 15N) of benthic organisms provides a useful solution to this problem. Through a 7-yr monitoring effort in Quintana Roo, Mexico, we show that δ 15N values of the common sea fan Gorgonia ventalina were more variable near a developed (Akumal) site than at an undeveloped (Mahahual) site. Beginning in 2007, the global recession decreased tourist visitations to Akumal, which corresponded with a pronounced 1.6 ‰ decline in sea fan δ 15N through 2009, at which time δ 15N values were similar to those from Mahahual. With the recovery of tourism, δ 15N values increased to previous levels. Overall, 84 % of the observed variation in δ 15N was explained by tourist visitations in the preceding year alone, indicating that variable nitrogen source contributions are correlated with sea fan δ 15N values. We also found that annual precipitation accounted for some variation in δ 15N, likely due to its role in groundwater flushing into the sea. Together, these factors accounted for 96 % of the variation in δ 15N. Using a mixing model, we estimate that sewage can account for up to 42 % of nitrogen in sea fan biomass. These findings illustrate the high connectivity between land-based activities and coral reef productivity and the measurable impact of the tourism industry on the ecosystem it relies on.

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References

  • ArandaCireol N, Herrera-Silveira JA, Comin FA (2006) Nutrient water quality in a tropical coastal zone with groundwater discharge, northwest Yucatan, Mexico. Estuar Coast Shelf Sci 68:445–454

    Article  Google Scholar 

  • Back W, Hanshaw BB, Pyle TE, Plummer LN, Weidie AE (1979) Geochemical significance of groundwater discharge and carbonate solution to the formation of Caleta Xel Ha, Quintana Roo, Mexico. Water Resour Res 15:1521–1535

    Article  CAS  Google Scholar 

  • Baker DM, Webster KL, Kim K (2010a) Caribbean octocorals record changing carbon and nitrogen sources from 1862 to 2005. Global Change Biol 16:2701–2710

    Article  Google Scholar 

  • Baker DM, Jordán-Dahlgren E, Maldonado MA, Harvell CD (2010b) Sea fan corals provide a stable isotope baseline for assessing sewage pollution in the Mexican Caribbean. Limnol Oceanogr 55:2139–2149

    Article  CAS  Google Scholar 

  • Baker DM, Kim K, Andras JP, Sparks JP (2011) Light-mediated 15N fractionation in Caribbean gorgonian octocorals: implications for pollution monitoring. Coral Reefs 30:709–717

    Article  Google Scholar 

  • Bauer-Gottwein P, Gondwe BRN, Charvet G, Marín LE, Rebolledo-Vieyra M, Merediz-Alonso G (2011) Review: The Yucatán Peninsula karst aquifer, Mexico. Hydrogeology J 19:507–524

    Article  Google Scholar 

  • Carruthers T, Vantussenbroek B, Dennison W (2005) Influence of submarine springs and wastewater on nutrient dynamics of Caribbean seagrass meadows. Estuar Coast Shelf Sci 64:191–199

    Article  Google Scholar 

  • Cervantes Martínez A (2007) El balance hídrico en cuerpos de agua cársticos de la Península de Yucatan. Teoría y Praxis 3:143–152

    Google Scholar 

  • Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28:589–606

    Article  Google Scholar 

  • Costanzo SD, Murby J, Bates J (2005) Ecosystem response to antibiotics entering the aquatic environment. Mar Pollut Bull 51:218–223

    Article  PubMed  CAS  Google Scholar 

  • Fabricius K (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  PubMed  CAS  Google Scholar 

  • Fogel ML, Wooler MJ, Cheeseman J, Smallwood BJ, Roberts Q, Romero I, Jacobsen Meyers M (2008) Unusually negative nitrogen isotopic compositions (δ 15N) of mangroves and lichens in an oligotrophic, microbially influenced ecosystem. Biogeosciences Discussions 5:937–969

    Article  Google Scholar 

  • Fourqurean J, Escorcia S, Anderson W, Zieman JC (2005) Spatial and seasonal variability in elemental content, δ 13C, and δ 15N of Thalassia testudinum from South Florida and its implications for ecosystem studies. Estuaries 28:447–461

    Article  CAS  Google Scholar 

  • Furnas M, Mitchell A, Skuza M, Brodie J (2005) The other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar Pollut Bull 51:253–265

    Article  PubMed  CAS  Google Scholar 

  • Gartner A, Lavery P, Smit AJ (2002) Use of δ 15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal. Mar Ecol Prog Ser 235:63–73

    Article  Google Scholar 

  • Heaton T (1986) Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chem Geol 59:87–102

    Article  CAS  Google Scholar 

  • Hernández-Terrones L, Rebolledo-Vieyra M, Merino-Ibarra M, Soto M, Le-Cossec A, Monroy-Rios E (2011) Groundwater pollution in a karstic region (NE Yucatan): Baseline nutrient concentrations and flux to coastal ecosystems. Water Air Soil Pollut 218:517–528

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  PubMed  CAS  Google Scholar 

  • INEGI (2011) Censo de Población y Vivienda 2010. Tabulados Básicos. Quintana Roo, México, INEGI. http://www.censo2010.org.mx/ Accessed 2011 Nov 23

  • Jones R, Boyer J (2000) Florida Keys National Marine Sanctuary: Water Quality Monitoring Project FY2000 Annual Report. Southeast Environmental Research Center, Florida International University

  • Kaczmarsky LT, Draud M, Williams EH (2005) Is there a relationship between proximity to sewage effluent and the prevalence of coral disease? Caribb J Sci 41:124–137

    Google Scholar 

  • Karl D, Letelier R, Tupas L, Dore J, Christian J, Hebel D (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388:533–538

    Article  CAS  Google Scholar 

  • Lapointe BE, Thacker K, Hanson C, Getten L (2011) Sewage pollution in Negril, Jamaica: effects of nutrition and ecology of coral reef macroalgae. Chin J Oceanol Limnol 29:775–789

    Article  CAS  Google Scholar 

  • Leichter J, Stewart H, Miller S (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407

    Article  Google Scholar 

  • Marion G, Dunbar R, Mucciarone D, Kremer JN, Lansing SJ, Arthawiguna A (2005) Coral skeletal δ 15N reveals isotopic traces of an agricultural revolution. Mar Pollut Bull 50:931–944

    Article  PubMed  CAS  Google Scholar 

  • McClelland JW, Valiela I, Michener RH (1997) Nitrogen stable isotope signatures in estuarine food webs: A record of increasing urbanization in coastal watersheds. Limnol Oceanogr 42:930–937

    Article  CAS  Google Scholar 

  • Metcalfe CD, Beddows PA, Bouchot GG et al (2011) Contaminants in the coastal karst aquifer system along the Caribbean coast of the Yucatan Peninsula, Mexico. Environ Pollut 159:991–997

    Article  PubMed  CAS  Google Scholar 

  • Moynihan M, Baker D, Mmochi A (2012) Isotopic and microbial indicators of sewage pollution from Stone Town, Zanzibar, Tanzania. Mar Pollut Bull 64:1348–1355

    Article  PubMed  CAS  Google Scholar 

  • Murray G (2007) Constructing paradise: The impacts of big tourism in the Mexican coastal zone. Coast Manage 35:339–355

    Article  Google Scholar 

  • Mutchler T, Dunton K, Townsend-Small A, Fredriksen S, Rasser M (2007) Isotopic and elemental indicators of nutrient sources and status of coastal habitats in the Caribbean Sea, Yucatan Peninsula, Mexico. Estuar Coast Shelf Sci 74:449–457

    Article  Google Scholar 

  • Pacheco J, Marin L, Cabrera A, Steinich B, Escolero O (2001) Nitrate temporal and spatial patterns in 12 water-supply wells, Yucatan, Mexico. Environ Geol 40:708–715

    Article  CAS  Google Scholar 

  • Patterson KL, Porter JW, Ritchie KB, Polson SW, Mueller E, Peters EC, Santavy DL, Smith GW (2002) The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci USA 99:8725–8730

    Article  PubMed  CAS  Google Scholar 

  • Risk MJ (2009) The reef crisis and the reef science crisis: nitrogen isotopic ratios as an objective indicator of stress. Mar Pollut Bull 58:787–788

    Article  PubMed  CAS  Google Scholar 

  • Risk MJ, Lapointe BE, Sherwood OA, Bedford BJ (2009) The use of δ 15N in assessing sewage stress on coral reefs. Mar Pollut Bull 58:793–802

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Martínez RE, Jordán-Garza AG, Baker DM, Jordán-Dahlgren E (2012) Competitive interactions between corals and Trididemnum solidum on Mexican Caribbean reefs. Coral Reefs 31:571–577

    Article  Google Scholar 

  • Savage C, Elmgren R (2004) Macroalgal (Fucus vesiculosis) δ 15N values trace decrease in sewage influence. Ecol Appl 14:517–526

    Article  Google Scholar 

  • SECTUR (2011) http://datatur.sectur.gob.mx/wb/datatur/reportes_datatur Accessed 2011 Oct 10

  • SEIGE (2012) http://seplader.seige.qroo.gob.mx/seigeweb/Anuarios.php Accessed 2012 Mar 3

  • Sherwood OA, Lapointe BE, Risk MJ, Jamieson RE (2010) Nitrogen isotopic records of terrestrial pollution encoded in Floridian and Bahamian gorgonian corals. Environ Sci Technol 44:874–880

    Article  PubMed  CAS  Google Scholar 

  • Smart PL, Beddows PA, Coke J, Doerr S, Smith S, Whitaker FF (eds) (2006) Special Paper 404: Perspectives on karst geomorphology, hydrology, and geochemistry - A tribute volume to Derek C. Ford and William B. White. Geological Society of America [doi:10.1130/2006.2404(10)]

  • Smith S, Kimmerer W, Laws E, Brock RE, Walsh T (1981) Kaneohe Bay sewage diversion experiment - perspectives on ecosystem responses to nutritional perturbation. Pac Sci 35:279–402

    CAS  Google Scholar 

  • Villasuso MJ, Méndez RR (2000) A conceptual model of the aquifer of the Yucatán Peninsula. In: Lutz W, Prieto L, Sanderson W (eds) Population, development, and environment on the Yucatán Peninsula: From ancient Maya to 2030. International Institute for Applied Systems Analysis, Laxenburg, Austria, pp 120–139

    Google Scholar 

  • Walker DI, Ormond RFG (1982) Coral death from sewage and phosphate pollution at Aqaba, Red Sea. Mar Pollut Bull 13:21–25

    Article  Google Scholar 

  • Ward-Paige CA, Risk MJ, Sherwood OA (2005) Reconstruction of nitrogen sources on coral reefs: δ 15N and δ 13C in gorgonians from Florida reef tract. Mar Ecol Prog Ser 296:155–163

    Article  CAS  Google Scholar 

  • Williams B, Risk MJ, Ross S, Sulak KJ (2006) Deep-water antipatharians: Proxies of environmental change. Geology 34:773–776

    Article  Google Scholar 

  • Yoshioka PM, Yoshioka BB (1991) A comparison of the survivorship and growth of shallow-water gorgonian species of Puerto Rico. Mar Ecol Prog Ser 69:253–260

    Article  Google Scholar 

  • Zurita F, Roy D, White J (2012) Municipal wastewater treatment in Mexico: Current status and opportunities for employing ecological treatment systems. Environ Tech 33:1151–1158

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Special thanks to CD Harvell, E Jordán-Dahlgren, MA Maldonado, AG Jordán-Garza, L. Vázquez, P Sánchez-Navarro, and the Centro Ecológico Akumal for logistical support. J García Barbabosa and the staff of Bucaneros del Caribe, and the staff of La Posada de los 40 Cañones assisted with sample collection in Mahahual. We thank CW Kwan for statistical advising. This work was supported by the Coral Disease Working Group of the Global Environment Facility Coral Targeted Research program, the W.M. Keck Foundation to MLF, a U.S. Environmental Protection Agency Science to Achieve Results fellowship to DMB, and a Smithsonian Marine Science Network Fellowship to DMB. The authors claim no conflict of interest with this work.

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  1. D. M. Baker

    Present address: School of Biological Sciences, The University of Hong Kong, Pokfulam Rd., Hong Kong, People’s Republic of China

Authors and Affiliations

  1. Smithsonian Institution, Marine Science Network, National Museum of Natural History, 1000 Constitution Ave., NW, Washington, DC, 20004, USA

    D. M. Baker

  2. Geophysical Laboratory, Carnegie Institution of Washington, 5251 Broad Branch Rd., NW, Washington, DC, 20015, USA

    D. M. Baker & M. L. Fogel

  3. Unidad Académica Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ap. Postal 1152, 77500, Cancún, QR, México

    R. E. Rodríguez-Martínez

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  3. M. L. Fogel
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Correspondence to D. M. Baker.

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Baker, D.M., Rodríguez-Martínez, R.E. & Fogel, M.L. Tourism’s nitrogen footprint on a Mesoamerican coral reef. Coral Reefs 32, 691–699 (2013). https://doi.org/10.1007/s00338-013-1040-2

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