Skip to main content

Advertisement

SpringerLink
Log in

Isotopic and Elemental Composition of Marine Macrophytes as Biotracers of Nutrient Recycling Within a Coastal Lagoon in Baja California, Mexico

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Nutrient sources of San Quintin Bay, a coastal lagoon affected by coastal upwelling off Baja California (Mexico), were traced using generalized additive (mixed) models (GAMM) to the stable nitrogen isotopic composition, C:N and N content of two co-occurring macrophytes (the macroalgae Ulva spp. and the seagrass Zostera marina). The geochemical tracers followed a spatial trend that partly responded to the long-term nutrient gradient from the ocean towards the interior of the bay. N content in Z. marina and Ulva spp. decreased linearly (while C:N increased) towards the middle section of the bay to concentration levels that indicate potential N limitation for growth. Concurrently midway into the bay (6–9 km), the δ15N of both macrophytes showed a gradual enrichment in 15N reflecting progressive denitrification. The spatial pattern of δ15N and the decrease in C:N of the macrophytes towards the innermost section of the bay indicated an additional nonoceanic source of dissolved nitrogen in this zone. The similarity of the δ15N pattern of Z. marina and Ulva spp. implies that their δ15N composition is mainly controlled by the availability of N, in spite of the physiological differences between taxa. A better fit of GAMM to N content and C:N was obtained for Z. marina than for Ulva spp. indicating that the former delineate more steadily and smoothly the influence of upwelling along the spatial gradient. Nonetheless, Ulva spp. may be analyzed in combination with Z. marina to characterize the environmental conditions at the time of sampling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Aguiar A.B., J.A. Morgan, M. Teichberg, S. Fox, and I. Valiela. 2003. Transplantation and isotopic evidence of the relative effects of ambient and internal nutrient supply on the growth of Ulva lactuca. The Biological Bulletin 205: 250–251.

    Article  CAS  Google Scholar 

  • Aguirre-Muñoz A., R.W. Buddemeier, V.F. Camacho-Ibar, J.D. Carriquiry, S.E. Ibarra-Obando, B.W. Massey, S.V. Smith, and F. Wulff. 2001. Sustainability of coastal resource use in San Quintin, Mexico. Ambio 30: 142–149.

    Article  Google Scholar 

  • Alvarez-Borrego J., and S. Alvarez-Borrego. 1982. Temporal and spatial variability of temperature in two coastal lagoons. Reports of California Cooperative Oceanic Fisheries Investigations 23: 188–197.

    Google Scholar 

  • Alvarez-Borrego S. 2004. Nutrient and phytoplankton dynamics in a coastal lagoon strongly affected by coastal upwelling. Ciencias Marinas 30: 1–19.

    Google Scholar 

  • Atkinson M.J., and S.V. Smith. 1983. C:N:P ratios of benthic marine plants. Limnology and Oceanography 28: 568–574.

    Article  CAS  Google Scholar 

  • Bakun A., and C.S. Nelson. 1977. Climatology of upwelling related processes off Baja California. Reports of California Cooperative Oceanic Fisheries Investigations 19: 107–127.

    Google Scholar 

  • Bannon R.O., and C.T. Roman. 2008. Using stable isotopes to monitor anthropogenic nitrogen inputs to estuaries. Ecological Applications 18: 22–30.

    Article  Google Scholar 

  • Barrón C., J.J. Middelburg, and C.M. Duarte. 2006. Phytoplankton trapped within seagrass (Posidonia oceanica) sediments are a nitrogen source: an in situ isotope labeling experiment. Limnology and Oceanography 51: 1648–1653.

    Article  Google Scholar 

  • Bivand R.S., E.J. Pebesma, and V. Gomez-Rubio. 2008. Applied spatial data analysis with R. New York: Springer.

    Google Scholar 

  • Camacho-Ibar V.F., J.D. Carriquiry, and S.V. Smith. 2003. Non-conservative P and N fluxes and net ecosystem production in San Quintin Bay, Mexico. Estuaries 26: 1220–1237.

    Article  CAS  Google Scholar 

  • Camacho-Ibar, V.F., J.M. Hernández-Ayón, E.M. Santamaría del Ángel, L.W. Daesslé-Heuser, and, J.A. Zertuche-González. 2007. Relación de las surgencias con los stocks de carbono en Bahía San Quintín, una Laguna costera del NW de México. In: Carbono en ecosistemas acuáticos de México, eds. B. Hernández dela Torre, and G. Gaxiola Castro, 355–370. Ensenada: Secretaría de Medio Ambiente y Recursos Naturales; Instituto Nacional de Ecología; Centro de Investigación Científica y de Educación Superior de Ensenada.

  • Caso M., C. Gonzalez-Abraham, and E. Ezcurra. 2007. Divergent ecological effects of oceanographic anomalies on terrestrial ecosystems of the Mexican Pacific coast. Proceedings of the National Academy of Sciences 104: 10530–10535.

    Article  CAS  Google Scholar 

  • Cifuentes L., M. Fogel, J. Pennock, and J. Sharp. 1989. Biogeochemical factors that influence the stable nitrogen isotope ratio of dissolved ammonium in the Delaware Estuary. Geochimica et Cosmochimica Acta 53: 2713–2721.

    Article  CAS  Google Scholar 

  • Cole M.L., I. Valiela, K.D. Kroeger, G.L. Tomasky, J. Cebrian, C. Wigand, R.A. McKinney, S.P. Grady, and M.H.C. da Silva. 2004. Assessment of a δ15N isotopic method to indicate anthropogenic eutrophication in aquatic ecosystems. Journal of Environmental Quality 33: 124–132.

    Article  CAS  Google Scholar 

  • Comisión Estatal del Agua de Baja California. 2008. Programa estatal hídrico 2008–2013 (Baja California Sate Water Board 2008–2013), 159 pp.

    Google Scholar 

  • Cook P.L.M., V. Evrad, and R.J. Woodland. 2015. Factors controlling nitrogen fixation in temperate seagrass beds. Marine Ecology Progress Series 525: 41–51.

    Article  CAS  Google Scholar 

  • Cornelisen C.D., S.R. Wing, K.L. Clark, M.H. Bowman, R.D. Frew, and C.L. Hurd. 2007. Patterns in the δ13C and δ15N signature of Ulva pertusa: interaction between physical gradients and nutrient source pools. Limnology and Oceanography 52: 820–832.

    Article  Google Scholar 

  • Daskin J.H., K.R. Calci, I.W. Burkhardt, and R.H. Carmichael. 2008. Use of N stable isotope and microbial analyses to define wastewater influence in Mobile Bay, AL. Marine Pollution Bulletin 56: 860–868.

    Article  CAS  Google Scholar 

  • Duarte C.M. 1990. Seagrass nutrient content. Marine Ecology Progress Series 6: 201–207.

    Article  Google Scholar 

  • Duarte C.M. 1992. Nutrient concentration of aquatic plants: patterns across species. Limnology and Oceanography 37: 882–889.

    Article  CAS  Google Scholar 

  • Fertig B., T.J.B. Carruthers, W.C. Dennison, A.B... Jones, F. Pantus, and B. Longstaff. 2009. Oyster and macroalgae bioindicators detect elevated δ15N in Maryland’s coastal bays. Estuaries and Coasts 32: 773–786.

    Article  CAS  Google Scholar 

  • Fourqurean J.W., T.O. Moore, B. Fry, and J.T. Hollibaugh. 1997. Spatial and temporal variation in C:N:P ratios, δ15N and δ13C of eelgrass Zostera marina as indicators of ecosystem processes, Tomales Bay, California, USA. Marine Ecology Progress Series 157: 147–157.

    Article  CAS  Google Scholar 

  • Hernández-Ayón J.M., M.S. Galindo-Bect, V.F. Camacho-Ibar, Z. García-Esquivel, M.A. González-Gómez, and F. Ley-Lou. 2004. Nutrient dynamics in the west arm of San Quintín Bay, Baja California, Mexico, during and after El Niño 1997/1998. Ciencias Marinas 30: 119–132.

    Google Scholar 

  • Hernández-Ayón J.M., V.F. Camacho-Ibar, A. Mejía-Trejo, and A. Cabello-Pasini. 2007. Variabilidad del CO2 total durante eventos de surgencia en Bahía San Quintín, Baja California, México. In Carbono en ecosistemas acuáticos de México, eds. B. Hernández de la Torre, andG. Gaxiola Castro, 187–200. Ensenada: Secretaría de Medio Ambiente y Recursos Naturales; Instituto Nacional de Ecología; Centro de Investigación Científica y de Educación Superior de Ensenada.

  • Hernández-Sánchez O.G. 2014. Identificación de las fuentes de nitrógeno para pastos marinos y macroalgas en bahía de San Quintín bajo condiciones de surgencias y no surgencia mediante análisis de isótopos estables de nitrógeno. MSc. Thesis, Marine Ecology Department, Centro de Investigación Científica y de Educación Superior de Ensenada unpublished.

  • Huntington B.E., and K.E. Boyer. 2008. Evaluating patterns of nitrogen supply using macroalgal tissue content and stable isotopic signatures in Tomales Bay, CA. Environmental Bioindicators 3: 180–192.

    Article  CAS  Google Scholar 

  • Ibarra-Obando S.E., S.V. Smith, M. Poumian-Tapia, V.F. Camacho-Ibar, J.D. Carriquiry, and M.A. Montes-Hugo. 2004. Benthic metabolism in San Quintin Bay, Baja California, Mexico. Marine Ecology Progress Series 283: 99–112.

    Article  CAS  Google Scholar 

  • Jorgensen P., S.E. Ibarra-Obando, and J.D. Carriquiry. 2007. Top-down and bottom-up stabilizing mechanisms in eelgrass meadows differentially affected by coastal upwelling. Marine Ecology Progress Series 333: 81–93.

    Article  Google Scholar 

  • Jorgensen P., S.E. Ibarra-Obando, and J.D. Carriquiry. 2010. Management of natural Ulva spp. blooms in San Quintin Bay, Baja California: is it justified?. Journal of Applied Phycology 22: 549–558.

    Article  Google Scholar 

  • Lehmann M.F., D.M. Sigman, D.C. McCorkle, J. Granger, S. Hoffmann, G. Cane, and B.G. Brunelle. 2007. The distribution of nitrate 15N/14N in marine sediments and the impact of benthic nitrogen loss on the isotopic composition of oceanic nitrate. Geochimica et Cosmochimica Acta 71: 5384–5404.

    Article  CAS  Google Scholar 

  • Marbà N., M.A. Hemminga, M.A. Mateo, C.M. Duarte, Y.E.M. Mass, J. Terrados, and E. Gacia. 2002. Carbon and nitrogen translocation between seagrass ramets. Marine Ecology Progress Series 226: 287–300.

    Article  Google Scholar 

  • McGlathery K.J., N. Risgaard-Petersen, and P.B. Christensen. 1998. Temporal and spatial variation in nitrogen fixation activity in the eelgrass Zostera marina rhizosphere. Marine Ecology Progress Series 168: 245–258.

    Article  CAS  Google Scholar 

  • Millán-Núñez R., S. Alvarez-Borrego, and D.M. Nelson. 1982. Effects of physical phenomena on the distribution of nutrients and phytoplankton productivity in a coastal lagoon. Estuarine, Coastal and Shelf Science 15: 317–335.

    Article  Google Scholar 

  • Papadimitriou S., H. Kennedy, D.P. Kennedy, and J. Borum. 2005. Seasonal and spatial variation in the organic carbon and nitrogen concentration and their stable isotopic composition in Zostera marina (Denmark). Limnology and Oceanography 50: 1084–1095.

    Article  CAS  Google Scholar 

  • Pebesma E.J. 2004. Multivariable geostatistics in S: the gstat package. Computational Geosciences 30: 683–691.

    Article  Google Scholar 

  • Pedersen M.F., and J. Borum. 1996. Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Marine Ecology Progress Series 142: 261–272.

    Article  CAS  Google Scholar 

  • Pedersen M.F., and J. Borum. 1997. Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Marine Ecology Progress Series 161: 155–163.

    Article  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and the R Development Core Team. 2013. nlme: linear and nonlinear mixed effects models. R package version 3.1–109.

  • R Core Team. 2013. R: a language and environment for statistical computing. Vienna: URL: http://www.R-project.org/ R Foundation for Statistical Computing.

    Google Scholar 

  • Ribas-Ribas, M., J.M. Hernández-Ayón, V.F. Camacho-Ibar, A. Cabello-Pasini, A. Mejia-Trejo, R. Durazo, S. Galindo-Bect, A.J. Souza, J.M. Forja., and A. Siqueiros-Valencia. 2011. Effects of upwelling, tides and biological processes on the inorganic carbon system of a coastal lagoon in Baja California. Estuarine, Coastal and Shelf Science 95:367-376.

  • Rodríguez-Cardozo L. 2004. Evaluación del nitrógeno orgánico disuelto en los balances de nitrógeno en Bahía San Quintin, B.C., B.S. Thesis. Ensenada, Baja California: unpublish. Universidad Autónoma de Baja California.

    Google Scholar 

  • Sigman D.M., R. Robinson, A.N. Knapp, A. van Geen, D.C. McCorkle, J.A. Brandes, and R.C. Thunell. 2003. Distinguishing between water column and sedimentary denitrification in the Santa Barbara Basin using the stable isotopes of nitrate. Geochemistry, Geophysics, Geosystems 4: 1040–1060.

    Article  Google Scholar 

  • Tyler A.C., K.J. McGlathery, and S.A. Macko. 2005. Uptake of urea and amino acids by the macroalgae Ulva lactuca (Chlorophyta) and Gracilaria vermiculophyla (Rhodophyta). Marine Ecology Progress Series 294: 161–172.

    Article  CAS  Google Scholar 

  • Vonk J.A., J.J. Middelburg, J. Stapel, and T.J. Bouma. 2008. Dissolved organic nitrogen uptake by seagrasses. Limnology and Oceanography 53: 542–548.

    Article  CAS  Google Scholar 

  • Ward D.H., A. Morton, T.L. Tibbitts, D.C. Douglas, and E. Carrera-González. 2003. Long-term change in eelgrass distribution at Bahia San Quintin, Baja California, Mexico, using satellite imagery. Estuaries 26: 1529–1539.

    Article  Google Scholar 

  • Ward D.H., T.L. Tibbitts, A. Morton, E. Carrera-González, and R. Kempka. 2004. Use of digital multispectral videography to assess seagrass distribution in San Quintín Bay, Baja California, Mexico. Ciencias Marinas 30: 57–70.

    Google Scholar 

  • Welsh D.T. 2000. Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions and significance to primary productivity. Ecology Letters 3: 58–71.

    Article  Google Scholar 

  • West J.B., G.J. Bowen, T.E. Cerling, and J.R. Ehleringer. 2006. Stable isotopes as one of nature’s ecological recorders. Trends in Ecology & Evolution 21: 408–414.

    Article  Google Scholar 

  • Wood S.N. 2006. Generalized additive models: an introduction with R. New York: Chapman and Hall/CRC.

    Google Scholar 

  • Zertuche-González J.A., V.F. Camacho-Ibar, I. Pacheco-Ruíz, A. Cabello-Pasini, L.A. Galindo-Bect, J.M. Guzmán-Calderón, V. Macias-Carranza, and J. Espinoza-Ávalos. 2009. The role of Ulva spp. as a temporary nutrient sink in a coastal lagoon with oyster cultivation and upwelling influence. Journal of Applied Phycology 21: 729–736.

    Article  Google Scholar 

  • Zuur A.F., E.N. Ieno, N.J. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.

    Book  Google Scholar 

Download references

Acknowledgments

This study was partially funded by a Consejo Nacional de Ciencia y Tecnología (CONACYT) grant 134381 to SEIO and from internal funds from Universidad Autónoma de Baja California (UABC) to JDCB. We thank Victor Camacho for sharing the hydrological data presented in this study, derived from previously published work (cited therein). We thank Victor Camacho and Stephen V. Smith for the valuable comments to an early version of this paper. Eduardo Ortiz provided valuable help in the field and in the lab. We also thank Vicente and Vicentito Guerrero, Agromarinos, and Ostiones Guerrero for their valuable logistic support in the field. This work benefited greatly from helpful suggestions made by Ken Dunton and two anonymous reviewers, for whom we are grateful. Likewise, we are enormously grateful to Cathy Harris who kindly accepted to copyedit this document.

Author information

Authors and Affiliations

  1. Instituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja California, Apdo. Postal # 453, C.P. 22830, Ensenada, Baja California, Mexico

    José D. Carriquiry & Julio A. Villaescusa

  2. CICESE, Carretera Ensenada-Tijuana, No. 3918, C.P. 22860, Ensenada, Baja California, Mexico

    Pablo Jorgensen & Silvia E. Ibarra-Obando

Authors
  1. José D. Carriquiry
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pablo Jorgensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julio A. Villaescusa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvia E. Ibarra-Obando
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José D. Carriquiry.

Additional information

Communicated by Kenneth Dunton

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carriquiry, J.D., Jorgensen, P., Villaescusa, J.A. et al. Isotopic and Elemental Composition of Marine Macrophytes as Biotracers of Nutrient Recycling Within a Coastal Lagoon in Baja California, Mexico. Estuaries and Coasts 39, 451–461 (2016). https://doi.org/10.1007/s12237-015-9992-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-015-9992-9

Keywords

Search

Navigation