Abstract
Sediment porewater nutrients often occur at concentrations that are orders of magnitude higher than nutrients in overlying waters, and accordingly may subsidise growth of benthic macroalgal mats in estuarine ecosystems. The relative contribution of porewater nutrients is expected to be particularly important for macroalgae entrained in intertidal mudflat sediments, where access to water column nutrients is tidally constrained. In this study, filamentous Gracilaria chilensis thalli were simultaneously exposed to sediment and overlying water nutrient sources, labelled using 15N tracers (15NH4+ or 15NO3−) during a 5-day experiment. Dissolved inorganic N (DIN) uptake from porewater and overlying water accounted for 33 and 52%, respectively, of the N estimated as necessary to support the growth of G. chilensis, despite the two-fold lower DIN concentration of the overlying water and its periodic availability (8 h day−1). Of the total N assimilated by the plants, ~ 15% could not be accounted for, supporting the acquisition of other N forms in order to meet demand. We also found that regardless of background NH4+:NO3− ratios (i.e. 1:3 in overlying water and 12:1 in porewater), plants accumulated 15NH4+ significantly more readily than 15NO3−, indicating a preference for NH4+. This ability to utilise multiple sources and species of N relatively rapidly may partly explain the competitive success of entrained macroalgae relative to non-entrained species and historically abundant seagrass beds in these environments. These results underscore the significance of both internal nutrient loading and external inputs as important in sustaining opportunistic macroalgal blooms in shallow estuaries.





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Aldridge JN, Trimmer M (2009) Modelling the distribution and growth of “problem” green seaweed in the Medway estuary, UK J.H. Andersen and D.J. Conley [eds.]. Eutrophication Coast. Ecosyst. Towar. better Underst. Manag. Strateg. Sel. Pap. from Second Int. Symp. Res. Manag. Eutrophication Coast. Ecosyst. 20–23 June 2006, Nyborg, Denmark 207: 107–122. https://doi.org/10.1007/978-90-481-3385-7_10
Anderson IC, McGlathery KJ, Tyler AC (2003) Microbial mediation of “reactive” nitrogen transformations in a temperate lagoon. Mar Ecol Prog Ser 246:73–84. https://doi.org/10.3354/meps246073
Andría JR, Vergara J, Perez-Llorens JL (1999) Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cadiz, Spain, cultured under different inorganic carbon and nitrogen levels. Eur J Phycol 34:497–504. https://doi.org/10.1080/09541449910001718851
Beer S, Levy I (1983) Effects of photon fluence rate light spectrum composition on growth, photosynthesis pigment relations in Gracilaria sp. Blackwell, Hoboken
Berner RA (1980) Early diagenesis: a theortical approach. Princeton University Press, Princeton, NJ, p 241
Boucher G, Boucher-Rodoni R (1988) In situ measurement of respiratory metabolism and nitrogen fluxes at the interface of oyster beds. Mar Ecol Prog Ser 44:229–238. https://doi.org/10.3354/meps044229
Carnicas E, Jiménez C, Niell FX (1999) Effects of changes of irradiance on the pigment composition of Gracilaria tenuistipitata var. liui Zhang et Xia. J Photochem Photobiol B Biol 50:149–158. https://doi.org/10.1016/S1011-1344(99)00086-X
Ceccherelli G, Cinelli F (1997) Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymodocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay. J Exp Mar Bio Ecol 217:165–177. https://doi.org/10.1016/S0022-0981(97)00050-6
Churchland C, Weatherall A, Briones MJ, Grayston SJ (2012) Stable-isotope labeling and probing of recent photosynthates into respired CO2, soil microbes and soil mesofauna using a xylem and phloem stem injection technique on Sitka spruce (Picea sitchensis). Rapid Commun Mass Spectrom 26:2493–2501. https://doi.org/10.1002/rcm.6368
Corzo A, Van Bergeijk SA, García-Robledo E (2009) Effects of green macroalgal blooms on intertidal sediments: net metabolism and carbon and nitrogen contents. Mar Ecol Prog Ser 380:81–93. https://doi.org/10.3354/meps07923
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. https://doi.org/10.1126/science.1156401
Duarte CM (1995) Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:87–112. https://doi.org/10.1080/00785236.1995.10422039
Engelsen A, Hulth S, Pihl L, Sundba K (2008) Benthic trophic status and nutrient fluxes in shallow-water sediments. Estuar Coast Shelf Sci 78:783–795. https://doi.org/10.1016/j.ecss.2008.02.018
Fang HP, Zhang M, Zhang T, Chen J (2008) Predictions of nitrate diffusion in sediment using horizontal attenuated total reflection (HATR) by Fourier transform infrared (FTIR) spectrometry. Water Res 42:903–908. https://doi.org/10.1016/j.watres.2007.08.038
García-Robledo E, Corzo A (2011) Effects of macroalgal blooms on carbon and nitrogen biogeochemical cycling in photoautotrophic sediments: an experimental mesocosm. Mar Pollut Bull 62:1550–1556. https://doi.org/10.1016/j.marpolbul.2011.03.044
Gonen Y, Kimmel E, Tel-Or E, Friedlander M (1996) Intercellular assimilate translocation in Gracilaria cornea (Gracilariaceae, Rhodophyta). Hydrobiologia 326–327:421–428. https://doi.org/10.1007/BF00047841
Gonzalez DJ, Smyth AR, Piehler MF, McGlathery KJ (2013) Mats of the non-native macroalga, Gracilaria vermiculophylla, alter net denitrification rates and nutrient fluxes on intertidal mudflats. Limnol Oceanogr 58:2101–2108. https://doi.org/10.4319/lo.2013.58.6.2101
Green L, Sutula M (2014) How much is too much? Identifying benchmarks of adverse effects of macroalgae on the macrofauna in intertidal flats. Ecol Appl 24:300–314
Haglund K, Pedersén M (1993) Outdoor pond cultivation of the subtropical marine red alga Gracilaria tenuistipitata in brackish water in Sweden. Growth, nutrient uptake, co-cultivation with rainbow trout and epiphyte control. J Appl Phycol 5:271–284
Hanisak MD (1990) The use of Gracilaria tikvahiae (Gracilariales, Rhodophyta) as a model system to understand the nitrogen nutrition of culture seaweeds. Hydrobiologia 204(205):79–87
Hardison AK, Anderson IC, Canuel EA, Tobias CR, Veuger B (2011a) Carbon and nitrogen dynamics in shallow photic systems: interactions between macroalgae, microalgae, and bacteria. Limnol Oceanogr 56:1489–1503. https://doi.org/10.4319/lo.2011.56.4.1489
Hardison A, Tobias CR, Stanhope JW, Anderson IC, Canuel E (2011b) An experimental apparatus for laboratory and field-based perfusion of sediment porewater with dissolved tracers. Estuar Coasts 34:243–255. https://doi.org/10.1007/s12237-010-9285-2
Harrison PJ, Hurd CL (2001) Nutrient physiology of seaweeds: application of concepts to aquaculture. Cah Biol Mar 42:71–82
Hauxwell J, Cebrián J, Furlong C, Valiela I (2001) Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82:1007–1022
Hessing-Lewis ML, Hacker SD, Menge BA, McConville SO, Henderson J (2015) Are large macroalgal blooms necessarily bad? Nutrient impacts on seagrass in upwelling-influenced estuaries. Ecol Appl 25:1330–1347. https://doi.org/10.1890/14-0548.1.sm
Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472. https://doi.org/10.1046/j.1529-8817.2000.99139.x
Hurd CL, Berges JA, Osborne J, Harrison PJ (1995) An in vitro nitrate reductase assay for marine macroalgae - optimization and characterization of the enzyme for fucus-gardneri (Phaeophyta). J Phycol 31:835–843. https://doi.org/10.1111/j.0022-3646.1995.00835.x
Israel A, Beer S, Bowes G (1991) Photosynthetic carbon acquisition in the red alga Gracilaria conferta. Mar Biol 110:195–198. https://doi.org/10.1007/BF01313704
Kamer K, Fong P, Kennison RL, Schiff K (2004) The relative importance of sediment and water column supplies of nutrients to the growth and tissue nutrient content of the green macroalga Enteromorpha intestinalis along an estuarine resource gradient. Aquat Ecol 38:45–56. https://doi.org/10.1023/B:AECO.0000021041.31385.19
Kennison RL, Fong P (2014) Extreme eutrophication in shallow estuaries and lagoons of California is driven by a unique combination of local watershed modifications that trump variability associated with wet and dry seasons. Estuar Coasts 37:164–179. https://doi.org/10.1007/s12237-013-9687-z
Koch PL, Zachos JC, Gingerich PD (1992) Correlation between isotope records in marine and continental carbon reservoirs near the Palaeocene/Eocene boundary. Nature 358:319–322. https://doi.org/10.1038/358319a0
Krom MD, Berner RA (1980) The diffusion coefficients of sulfate, ammonium, and phosphate ions in anoxic marine sediments. Limnol Oceanogr 25:327–337. https://doi.org/10.4319/lo.1980.25.2.0327
Lavery PS, Oldham CE, Ghisalberti M (2001) The use of fick’s first law for predicting porewater nutrient fluxes under diffusive conditions. Hydrol Process 15:2435–2451. https://doi.org/10.1002/hyp.297
Lin X, Hou L, Liu M, Li X, Yin G, Zheng Y, Deng F (2016) Gross nitrogen mineralization in surface sediments of the Yangtze Estuary. PLoS ONE 11:1–16. https://doi.org/10.1371/journal.pone.0151930
Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Lomstein BA, Blackburn T, Henriksen K (1989) Aspects of nitrogen and carbon cycling in the northern Bering Shelf sediment. I. The significance of urea turnover in the mineralization of NH4+. Mar Ecol Prog Ser 57:237–247. https://doi.org/10.3354/meps057237
Lomstein BA, Jensen AGU, Hansen JW, Andreasen JB, Hansen LS, Berntsen J, Kunzendorf H (1998) Budgets of sediment nitrogen and carbon cycling in the shallow water of Knebel Vig, Denmark. Aquat Microb Ecol 14:69–80. https://doi.org/10.3354/ame014069
Magnien RE, Summers RM, Sellner KG (1992) External nutrient sources, internal nutrient pools, and phytoplankton production in Chesapeake Bay. Estuaries 15:497. https://doi.org/10.2307/1352393
McGlathery KJ, Krause-jensen D, Rysgaard S, Christensen PB (1997) Patterns of ammonium uptake within dense mats of the filamentous macroalga Chaetomorpha linum. Aquat Bot 59:99–115
Mitsch WJ, Gosselink JG (1993) Wetlands, 2nd edn. John Wiley, New York
Morris EP, Peralta G, Brun FG, van Duren L, Bouma TJ, Perez-Llorens JL (2008) Interaction between hydrodynamics and seagrass canopy structure: spatially explicit effects on ammonium uptake rates. Limnol Oceanogr 53:1531–1539. https://doi.org/10.4319/lo.2008.53.4.1531
Morris EP, Peralta G, Van Engeland T et al (2013) The role of hydrodynamics in structuring in situ ammonium uptake within a submerged macrophyte community. Limnol Oceanogr Fluids Environ 3:210–224. https://doi.org/10.1215/21573689-2397024
Naldi M, Wheeler PA (2002) 15 N measurements of ammonium and nitrate uptake by Ulva fenestrata (Chlorophyta) and Gracilaria pacifica (Rhodophyta): comparison of net nutrient disappearance, release of ammonium and nitrate, and 15 N accumulation in algal tissue. J Phycol 38:135–144. https://doi.org/10.1046/j.1529-8817.2002.01070.x
Navarro-Angulo L, Robledo D (1999) Effects of nitrogen source, N: P ratio and N-pulse concentration and frequency on the growth of Gracilaria cornea (Gracilariales, Rhodophyta) in culture. Hydrobiologia 398(399):315–320. https://doi.org/10.1023/A:1017099321188
Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391. https://doi.org/10.1016/j.aquaculture.2003.11.015
Ní Longphuirt S, O’Boyle S, Wilkes R, Dabrowski T, Stengel DB (2015) Influence of hydrological regime in determining the response of macroalgal blooms to nutrient loading in two irish estuaries. Estuar Coasts. https://doi.org/10.1007/s12237-015-0009-5
Nixon SW, Pilson MEQ (1983) Nitrogen in estuarine and coastal marine ecosystems. In: Carpenter EJ, Capone DJ (eds) Nitrogen in the marine environment. Plenum Press, New York, pp 565–648
Nyberg CD (2007) Introduced marine macroalgae and habitat modifiers: their ecological role and significant attributes. Mar Pollut Bull 55:323–332
Oviatt C, Doering P, Nowicki B, Reed L, Cole J, Frithsen J (1995) An ecosystem level experiment on nutrient limitation in temperate coastal marine environments. Oceanogr Lit Rev 42:763
Pedersen MF (1994) Transient ammonium uptake in the macroalga Ulva lactuca (Chlorophyta): regulation, and the consequences for choice of measuring technique. J Phycol 30:980–986
Pedersen MF, Borum J (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. Mar Ecol Prog Ser 142:261–272. https://doi.org/10.3354/meps142261
Pedersen A, Kraemer G, Yarish C (2004) The effects of temperature and nutrient concentrations on nitrate and phosphate uptake in different species of Porphyra from Long Island Sound (USA). J Exp Mar Bio Ecol 312:235–252. https://doi.org/10.1016/j.jembe.2004.05.021
Pickering TD, Gordon ME, Tong LJ (1990) Seasonal growth, density, reproductive phenology and agar quality of Gracilaria sordida (Gracilariales, Rhodophyta) at Mokomoko Inlet. N Z Hydrobiol 204(205):253–262
Pizarro A, Barrales H (1986) Field assessment of two methods for planting the agar-containing seaweed, Gracilaria, in Northern Chile. Aquaculture 59:31–43. https://doi.org/10.1016/0044-8486(86)90076-1
Reddy KR, Delaune RD (2008) Biogeochemistry of wetlands: science and applications. CRC Press, Boca Raton. https://doi.org/10.1201/9780203491454
Robertson BP, Savage C, Gardner JPA, Robertson BM, Stevens LM (2016) Optimising a widely-used coastal health index through quantitative ecological group classifications and associated thresholds. Ecol Indic. https://doi.org/10.1016/j.ecolind.2016.04.003
Rosenberg G, Ramus J (1984) Uptake of inorganic nitrogen and seaweed surface area: volume ratios. Aquat Bot 19:65–72. https://doi.org/10.1016/0304-3770(84)90008-1
Santelices B, Fonck E (1979) Ecologia y cultivo de Gracilaria lemaneiformis en Chile central. In: Santelices B (ed) Actas de1 Primer Simposium sobre Algas Marinas Chilenas. Sub- secretaria de Pesca, Ministerio de Economia, Foment0 y Reconstrnccion, Santiago, Chile, pp 165-200
Sanford LP, Crawford SM (2000) Mass transfer versus kinetic control of uptake across solid-water boundaries. Limnol Oceanogr 45:1180–1186. https://doi.org/10.4319/lo.2000.45.5.1180
Santelices B, Doty MS (1989) A review of Gracilaria farming. Aquaculture 78:95–133. https://doi.org/10.1016/0044-8486(89)90026-4
Santelices B, Vásquez J, Ohme U, Fonck E (1984) Managing wild crops of Gracilaria in central Chile, p. 77–89. In: Bird CJ, Ragan MA (eds.) Eleventh International Seaweed Symposium: Proceedings of the Eleventh International Seaweed Symposium, held in Qingdao, People’s Republic of China, June 19–25, 1983. Springer Netherlands
Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88. https://doi.org/10.1038/nature12860
Stein LY, Klotz MG (2011) Nitrifying and denitrifying pathways of methanotrophic bacteria. Biochem Soc Trans 39:1826–1831. https://doi.org/10.1042/BST20110712
Sundbäck K, Miles A, Hulth S, Pihl L, Engström P, Selander E, Svenson A (2003) Importance of benthic nutrient regeneration during initiation of macroalgal blooms in shallow bays. Mar Ecol Prog Ser 246:115–126
Sutula M, Green L, Cicchetti G, Detenbeck N, Fong P (2014) Thresholds of adverse effects of macroalgal abundance and sediment organic matter on benthic habitat quality in estuarine intertidal flats. Estuar Coasts 37(6):1532–1548. https://doi.org/10.1007/s12237-014-9796-3
Teichberg M, Fox SE, Aguila C, Olsen YS, Valiela I (2008) Macroalgal responses to experimental nutrient enrichment in shallow coastal waters: growth, internal nutrient pools, and isotopic signatures. Mar Ecol Prog Ser 368:117–126. https://doi.org/10.3354/meps07564
Teichberg M, Fox SE, Olsen Y et al (2010) Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Glob Change Biol 16:2624–2637. https://doi.org/10.1111/j.1365-2486.2009.02108.x
Touchette BW, Burkholder JM (2000) Review of nitrogen and phosphorus metabolism in seagrasses. J Exp Mar Bio Ecol 250:133–167
Trimmer M, Nedwell DB, Sivyer DB, Malcolm SJ (2000) Seasonal organic mineralisation and denitrification in intertidal sediments and their relationship to the abundance of Enteromorpha sp. and Ulva sp. Mar Ecol Prog Ser 203:67–80
Tyler A, McGlathery K, Anderson I (2001) Macroalgae mediation of dissolved organic nitrogen fluxes in a temperate coastal lagoon. Estuar Coast Shelf Sci 53:155–168. https://doi.org/10.1006/ecss.2001.0801
Tyler AC, McGlathery KJ, Anderson IC (2003) Benthic algae control sediment-water column fluxes of organic and inorganic nitrogen compounds in a temperate lagoon. Limnol Oceanogr 48:2125–2137. https://doi.org/10.4319/lo.2003.48.6.2125
Tyler AC, McGlathery KJ, Macko SA (2005) Uptake of urea and amino acids by the macroalgae Ulva lactuca (Chlorophyta) and Gracilaria vermiculophylla (Rhodophyta). Mar Ecol Prog Ser 294:161–172. https://doi.org/10.3354/meps294161
Valiela I, McClelland J, Hauxwell J, Behr P, Hersh D, Foreman K (1997) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42:1105–1118
van Katwijk M, Vergeer L, Schmitz G, Roelofs J (1997) Ammonium toxicity in eelgrass Zostera marina. Mar Ecol Prog Ser 157:159–173. https://doi.org/10.3354/meps157159
Wang C, Lei A, Zhou K, Hu Z, Hao W, Yang J (2014) Growth and nitrogen uptake characteristics reveal outbreak mechanism of the opportunistic Macroalga Gracilaria tenuistipitata. PLoS ONE 9(10):e108980. https://doi.org/10.1371/journal.pone.0108980
Weston NB, Giblin AE, Banta GT, Hopkinson CS, Tucker J (2010) The effects of varying salinity on ammonium exchange in estuarine sediments of the Parker River, Massachusetts. Estuar Coasts 33:985–1003. https://doi.org/10.1007/s12237-010-9282-5
Wheeler PA, Bjornsater BR (1992) Seasonal fluctuations in tissue nitrogen, phosphorus, and N: P for five macroalgal species common to the Pacific Northwest Coast. J Phycol 28:1–6. https://doi.org/10.1111/j.0022-3646.1992.00001.x
Williams SL (1984) Uptake of sediment ammonium and translocation in a marine green macroalga Caulerpa cupressoides. Limnol Oceanogr 29:374–379. https://doi.org/10.4319/lo.1984.29.2.0374
Acknowledgements
This research was supported by Environment Southland and Greater Wellington Regional Councils, Department of Conservation (NZ), New Zealand Coastal Society (PhD Research Grant), Botanical Society of Otago (Peter Bannister Student Field Grant) through research Grants, with additional support from the University of Otago (Doctoral scholarship). We would like to acknowledge Dr Barry Robertson, Robertson Environmental, for revealing the overall need for this work and helping with site selection, and Nick Ward, Environment Southland, for his support in the field. We also thank Professor Charles T. Driscoll and four anonymous reviewers whose comments greatly improved this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Charles T. Driscoll.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Robertson, B.P., Savage, C. Mud-entrained macroalgae utilise porewater and overlying water column nutrients to grow in a eutrophic intertidal estuary. Biogeochemistry 139, 53–68 (2018). https://doi.org/10.1007/s10533-018-0454-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-018-0454-x

