Advertisement

Estuaries and Coasts

, Volume 42, Issue 3, pp 731–742 | Cite as

Regulation of Nitrate Uptake by the Seagrass Zostera marina During Upwelling

  • José M. Sandoval-Gil
  • María del Carmen Ávila-López
  • Víctor F. Camacho-IbarEmail author
  • José Martín Hernández-Ayón
  • José A. Zertuche-González
  • Alejandro Cabello-Pasini
Article

Abstract

Prolonged nitrogen (N) fertilization can impact seagrass survival and productivity; however, the effects of N enrichment pulses (e.g., upwelling or sediment resuspension) remain poorly understood. This study examined the effects of short-term (1 h) pulsing of nitrate (NO3) enrichment, simulating an upwelling event, on dissolved inorganic carbon (DIC) and NO3 uptake capacities, critical in controlling eelgrass productivity. Zostera marina dominates submerged vegetation in coastal lagoons influenced by upwelling in the California Current system. Laboratory incubations were conducted in winter (non-upwelling) and spring (upwelling) with shoots collected from San Quintín Bay meadows, Baja California, Mexico, differentially exposed to upwelled NO3. Results suggest that NO3 enrichment stimulated DIC and NO3 uptake in winter, reflecting the close relationship between carbon metabolism and NO3 assimilation. Eelgrass shoots showed reduced NO3 incorporation in spring; neither NO3 uptake nor photosynthesis increased when exposed to high NO3. Saturation of spring shoots at lower ambient NO3 concentrations may be interpreted as a physiological strategy to restrict metabolically costly NO3 incorporation during upwelling; this regulation of NO3 uptake strongly contrasts to the apparently full exploitation of this nutrient by seaweeds also dominant within the bay, as indicated in previous works. Despite their reduced NO3 uptake, eelgrass meadows near the bay mouth acquire NO3 at rates up to 4.2 mmol N m−2 day−1. This represents non-trivial water column NO3 removal compared to the estimated oceanic NO3 supply (~ 7.1 mmol m−2 day−1) during upwelling, highlighting the importance of Z. marina beds in controlling the lagoonal N-budget.

Keywords

Zostera marina Upwelling Pulsed nitrate fertilization DIC uptake N uptake 

Notes

Acknowledgements

This research was funded by the National Council for Science and Technology (CONACYT, Mexico, project CB-2010-01-154376 awarded to VFCI). JMSG was supported by a postdoctoral grant from the Mexican Ministry of Public Education (SEP, PROMEP/103.5/13/5009). We are especially grateful to Julieta Hernández, Nevia Alfaro, and Jesús Galarza (IIO-UABC) for their technical support.

We sincerely thank two anonymous reviewers for their comments which helped to improve the final version of this manuscript.

References

  1. Alexandre, A., J. Silva, T.J. Bouma, and R. Santos. 2011. Inorganic nitrogen uptake kinetics and whole-plant nitrogen budget in the seagrass Zostera noltii. Journal of Experimental Marine Biology and Ecology 401 (1–2): 7–12.CrossRefGoogle Scholar
  2. Apostolaki, E.T., S. Vizzini, and I. Karakassis. 2012. Leaf vs. epiphyte nitrogen uptake in a nutrient enriched Mediterranean seagrass (Posidonia oceanica) meadow. Aquatic Botany 96 (1): 58–62.CrossRefGoogle Scholar
  3. Ávila-López, M.C., J.M. Hernández-Ayón, V.F. Camacho-Ibar, A.F. Bermúdez, A. Mejía-Trejo, I. Pacheco-Ruiz, and J.M. Sandoval-Gil. 2016. Air–water CO2 fluxes and net ecosystem production changes in a Baja California coastal lagoon during the anomalous North Pacific warm condition. Estuaries and Coasts 40 (3): 792–806.CrossRefGoogle Scholar
  4. Beer, S. 1994. Mechanisms of inorganic carbon acquisition in marine macroalgae (with special reference to the Chlorophyta). In Progress in phycological research, ed. F.E. Round and D.J. Chapman DJ, 179–207. Bristol, UK: Biopress.Google Scholar
  5. Beer, S., M. Bjork, F. Hellblom, and L. Axelsson. 2002. Inorganic carbon utilization in marine angiosperms (seagrasses). Functional Plant Biology 29 (3): 349–354.CrossRefGoogle Scholar
  6. Boudouresque, C. F., Bernard, G., Pergent, G., Shili, A., & Verlaque, M. 2009. Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Botanica Marina, 52(5), 395–418.Google Scholar
  7. Burkholder, J.M., K.M. Mason, and H.B. Glasgow Jr. 1992. Water column nitrate enrichment promotes decline of eelgrass (Zostera marina L.): Evidence from seasonal mesocosm experiments. Marine Ecology Progress Series 81: 163–178.CrossRefGoogle Scholar
  8. Burkholder, J. M., Glasgow Jr, H. B., & Cooke, J. E. 1994. Comparative effects of water-column nitrate enrichment on eelgrass Zostera marina, shoalgrass Halodule wrightii, and widgeongrass Ruppia maritima. Marine Ecology Progress Series, 121–138.Google Scholar
  9. Burkholder, J.M., D. Tomasko, and B.W. Touchette. 2007. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350 (1-2): 46–72.CrossRefGoogle Scholar
  10. Cabello-Pasini, A., C. Lara-Turrent, and R.C. Zimmerman. 2002. Effect of storms on photosynthesis, carbohydrate content and survival of eelgrass populations from a coastal lagoon and the adjacent open ocean. Aquatic Botany 74 (2): 149–164.CrossRefGoogle Scholar
  11. Cabello-Pasini, A., R. Muñiz-Salazar, and D.H. Ward. 2003. Annual variations of biomass and photosynthesis in Zostera marina at its southern end of distribution in the North Pacific. Aquatic Botany 76 (1): 31–47.CrossRefGoogle Scholar
  12. Cabello-Pasini, A., R. Muñiz-Salazar, and D.H. Ward. 2004. Biochemical characterization of the eelgrass Zostera marina at its southern distribution limit in the North Pacific. Ciencias Marinas 30 (1A): 21–34.CrossRefGoogle Scholar
  13. Camacho-Ibar, V.F., J.D. Carriquiry, and S.V. Smith. 2003. Non-conservative P and N fluxes and net ecosystem production in San Quintín Bay, Mexico. Estuaries 26 (5): 1220–1237.CrossRefGoogle Scholar
  14. Cornelisen, C.D., and F.I.M. Thomas. 2004. Ammonium and nitrate uptake by leaves of the seagrass Thalassia testudinum: Impact of hydrodynamic regime and epiphyte cover on uptake rates. Journal of Marine Systems 49 (1-4): 177–194.CrossRefGoogle Scholar
  15. Drechsler, Z., R. Sharkia, Z.I. Cabantchik, and S. Beer. 1994. The relationship of arginine groups to photosynthetic HCO3 -uptake in Ulva sp. mediated by a putative anion exchanger. Planta 194 (2): 250–255.CrossRefGoogle Scholar
  16. Duarte, C. M. 1990. Seagrass nutrient content. Marine Ecology Progress Series 67: 201–207.Google Scholar
  17. Fourqurean, J.W., T.O. Moore, B. Fry, and T.J. 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.CrossRefGoogle Scholar
  18. Hauxwell, J., J. Cebrián, and I. Valiela. 2003. Eelgrass Zostera marina loss in temperate estuaries: Relationship to land-derived nitrogen loads and effect of light limitation imposed by algae. Marine Ecology Progress Series 247: 59–73.CrossRefGoogle Scholar
  19. Hemminga, M.A., B.P. Koutstaal, J. van Soelen, and A.G.A. Merks. 1993. The nitrogen supply to intertidal eelgrass (Zostera marina). Marine Biology 118 (2): 223–227.CrossRefGoogle Scholar
  20. Hemminga, M.A., N. Marbá, and J. Stapel. 1999. Leaf nutrient resorption, leaf lifespan and the retention of nutrients in seagrass systems. Aquatic Botany 65 (1-4): 141–158.CrossRefGoogle Scholar
  21. Hernández-Ayón, J.M., S.L. Belli, and A. Zirino. 1999. pH, alkalinity and total CO2 in coastal seawater by potentiometric titration with a difference derivative readout. Analytica Chimica Acta 394 (1): 101–108.CrossRefGoogle Scholar
  22. Hernández-Ayón, J.M., S. Galindo-Bect, V.F. Camacho-Ibar, S. García- Esquivel, M.A. González-Gómez, and F. Ley-Lou. 2004. Nutrient dynamics in the west arm of San Quintín Bay, Baja California, Mexico. Ciencias Marinas 30 (1A): 119–132.CrossRefGoogle Scholar
  23. Hessing-Lewis, M.L., and S.D. Hacker. 2013. Upwelling influences, macrophyte blooms, and seagrass production; temporal trends from latitudinal and local scales in northeast Pacific estuaries. Limnology and Oceanography 58 (3): 1103–1112.CrossRefGoogle Scholar
  24. Hurd, C.L., P.J. Harrison, K. Bischof, and C.S. Lobban. 2014. Seaweed ecology and physiology. Cambridge: Cambridge University Press.Google Scholar
  25. Invers, O., J. Romero, and M. Pérez. 1997. Effects of pH on seagrass photosynthesis: A laboratory and field assessment. Aquatic Botany 59 (3-4): 185–194.CrossRefGoogle Scholar
  26. Invers, O., G.P. Kraemer, M. Pérez, and J. Romero. 2004. Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica. Journal of Experimental Marine Biology and Ecology 303 (1): 97–114.CrossRefGoogle Scholar
  27. Koch, M., G. Bowes, C. Ross, and X.H. Zhang. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19 (1): 103–132.CrossRefGoogle Scholar
  28. Kraemer, G. P., & Mazzella, L. 1999. Nitrogen acquisition, storage, and use by the co-occurring Mediterranean seagrasses Cymodocea nodosa and Zostera noltii. Marine Ecology Progress Series, 183, 95–103.Google Scholar
  29. Lee, K.-S., and K.H. Dunton. 1999. Inorganic nitrogen acquisition in the seagrass Thalassia testudinum: Development of a whole-plant nitrogen budget. Limnology and Oceanography 44 (5): 1204–1215.CrossRefGoogle Scholar
  30. Lepoint, G., S. Millet, P. Dauby, S. Gobert, and J.M. Bouquegneau. 2002. Annual nitrogen budget of the seagrass Posidonia oceanica as determined by in situ uptake experiments. Marine Ecology Progress Series 237: 87–96.CrossRefGoogle Scholar
  31. Longstaff, B.J., T. Kildea, J.W. Runcie, A. Cheshire, W.C. Dennison, C. Hurd, T. Kana, J. Raven, and A.W. Larkum. 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynthesis Research 74 (3): 281–293.CrossRefGoogle Scholar
  32. Marbá, N., M.A. Hemminga, M.A. Mateo, C.M. Duarte, Y. Mass, J. Terrados, and E. Gacia. 2002. Carbon and nutrient translocation between seagrass ramets. Marine Ecology Progress Series 226: 287–300.CrossRefGoogle Scholar
  33. Marín-Guirao, L., J.M. Sandoval-Gil, R. García-Muñoz, and J.M. Ruiz. 2017. The stenohaline seagrass Posidonia oceanica can persist in natural environments under fluctuating hypersaline conditions. Estuaries and Coasts 40 (6): 1688–1704.CrossRefGoogle Scholar
  34. McGlathery, K. J., Sundbäck, K., & Anderson, I. C. 2007. Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter. Marine Ecology Progress Series, 348, 1–18.Google Scholar
  35. 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 (4): 1084–1095.CrossRefGoogle Scholar
  36. Pedersen, M.F. 1994. Transient ammonium uptake in the macroalga Ulva lactuca (Chlorophyta): Nature, regulation, and the consequences for choice of measuring technique. Journal of Phycology 30 (6): 980–986.CrossRefGoogle Scholar
  37. Pedersen, M. F., & Borum, J. 1992. Nitrogen dynamics of eelgrass Zostera marina during low nutrient availability. Marine Ecology Progress Series, 80, 65–73.Google Scholar
  38. Pedersen, M. F., & Borum, J. 1993. An annual nitrogen budget for a seagrass Zostera marina population. Marine Ecology Progress Series, 101, 169–169.Google Scholar
  39. 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 (4): 367–376.CrossRefGoogle Scholar
  40. Rubio, L., Linares-Rueda, A., Garcia-Sanchez, M. J., & Fernández, J. A. 2007. Ammonium uptake kinetics in root and leaf cells of Zostera marina L. Journal of Experimental Marine Biology and Ecology, 352(2), 271–279.Google Scholar
  41. Ruiz, J.M., and J. Romero. 2001. Effects of in situ experimental shading on the Mediterranean seagrass Posidonia oceanica. Marine Ecology Progress Series 215: 107–120.CrossRefGoogle Scholar
  42. Ruiz, J.M., C. Marco-Méndez, and J.L. Sánchez-Lizaso. 2010. Remote influence of offshore fish farm waste on Mediterranean seagrass (Posidonia oceanica) meadows. Marine Environmental Research 69 (3): 118–126.CrossRefGoogle Scholar
  43. Ruesink, J.L., S. Yang, and A.C. Trimble. 2015. Variability in carbon availability and eelgrass (Zostera marina) biometrics along an estuarine gradient in Willapa Bay, WA, USA. Estuaries and Coasts 38 (6): 1908–1917.CrossRefGoogle Scholar
  44. Sandoval-Gil, J.M., V.F. Camacho-Ibar, M.C. Ávila-López, J. Hernández-López, J.A. Zertuche-González, and A. Cabello-Pasini. 2015. Dissolved inorganic nitrogen uptake kinetics and δ15N of Zostera marina L. (eelgrass) in a coastal lagoon with oyster aquaculture and upwelling influence. Journal of Experimental Marine Biology and Ecology 472: 1–13.CrossRefGoogle Scholar
  45. Sandoval-Gil, J., A. Alexandre, R. Santos, and V.F. Camacho-Ibar. 2016. Nitrogen uptake and internal recycling in Zostera marina exposed to oyster farming: Eelgrass potential as a natural biofilter. Estuaries and Coasts 39 (6): 1694–1708.CrossRefGoogle Scholar
  46. Stapel, J., T.L. Aarts, B.H.M. van Duynhoven, J.D. De Groot, P.H.W. van den Hoogen, and M.A. Hemminga. 1996. Nutrient uptake by leaves and roots of the seagrass Thalassia hemprichii in the Spermonde Archipelago, Indonesia. Marine Ecology Progress Series 134: 195–206.CrossRefGoogle Scholar
  47. Terrados, J., and S.L. Williams. 1997. Leaf versus root nitrogen uptake by the surfgrass Phyllospadix torreyi. Marine Ecology Progress Series 149: 267–277.CrossRefGoogle Scholar
  48. Touchette, B.W., and J.M. Burkholder. 2000. Review of nitrogen and phosphorus metabolism in seagrasses. Journal of Experimental Marine Biology and Ecology 250 (1-2): 133–167.CrossRefGoogle Scholar
  49. Touchette, B.W., and J.M. Burkholder. 2007. Carbon and nitrogen metabolism in the seagrass, Zostera marina L.: Environmental control of enzymes involved in carbon allocation and nitrogen assimilation. Journal of Experimental Marine Biology and Ecology 350 (1-2): 216–233.CrossRefGoogle Scholar
  50. Thursby, G.B., and M.M. Harlin. 1982. Leaf-root interaction in the uptake of ammonia by Zostera marina. Marine Biology 72 (2): 109–112.CrossRefGoogle Scholar
  51. Udy, J.W., and W.C. Dennison. 1997. Growth and physiological responses of three seagrass species to elevated sediment nutrients in Moreton Bay, Australia. Journal of Experimental Marine Biology and Ecology 217 (2): 253–277.CrossRefGoogle Scholar
  52. van Katwijk, M.M., L.H.T. Vergeer, G.H.W. Schimitz, and J.G.M. Roelofs. 1997. Ammonium toxicity in eelgrass Zostera marina. Marine Ecology Progress Series 157: 159–173.CrossRefGoogle Scholar
  53. Villazán, B., M.F. Pedersen, F.G. Brun, and J.J. Vergara. 2013. Elevated ammonium concentrations and low light form a dangerous synergy for eelgrass Zostera marina. Marine Ecology Progress Series 493: 141–154.CrossRefGoogle Scholar
  54. Villazán, B., T. Salo, F.G. Brun, J.J. Vergara, and M.F. Pedersen. 2015. High ammonium availability amplifies the adverse effect of low salinity on eelgrass Zostera marina. Marine Ecology Progress Series 536: 149–162.CrossRefGoogle Scholar
  55. Ward, D.H., A. Morton, T.L. Tibbitts, D.C. Douglas, and E. Carrera- González. 2003. Long-term change in eelgrass distribution at Bahía San Quintín, Baja California, Mexico, using satellite imagery. Estuaries 26 (6): 1529–1539.CrossRefGoogle Scholar
  56. Zertuche-González, J., V.F. Camacho-Ibar, I. Pacheco-Ruíz, A. Cabello-Pasini, L. Galindo-Bect, J. Guzmán-Calderón, V. Macías-Carranza, and J. Espinoza-Avalos. 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 (6): 729–736.CrossRefGoogle Scholar
  57. Zieman, J. C. 1974. Methods for the study of the growth and production of turtle grass, Thalassia testudinum König. Aquaculture, 4, 139–143.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2019

Authors and Affiliations

  • José M. Sandoval-Gil
    • 1
  • María del Carmen Ávila-López
    • 1
  • Víctor F. Camacho-Ibar
    • 1
    Email author
  • José Martín Hernández-Ayón
    • 1
  • José A. Zertuche-González
    • 1
  • Alejandro Cabello-Pasini
    • 1
  1. 1.Instituto de Investigaciones OceanológicasUniversidad Autónoma de Baja CaliforniaEnsenadaMexico

Personalised recommendations