Final Report: Developing an Indicator for Nutrient Supply in Tropical and Temperate Estuaries, Bays, and Coastal Waters Using the Tissue Nitrogen and Phosphorus Content of Macroalgae

EPA Grant Number: R827637
Title: Developing an Indicator for Nutrient Supply in Tropical and Temperate Estuaries, Bays, and Coastal Waters Using the Tissue Nitrogen and Phosphorus Content of Macroalgae
Investigators: Fong, Peggy
Institution: University of California - Los Angeles
EPA Project Officer: Hahn, Intaek
Project Period: August 1, 1999 through July 31, 2002
Project Amount: $399,335
RFA: Ecological Indicators (1999) RFA Text |  Recipients Lists
Research Category: Ecological Indicators/Assessment/Restoration , Ecosystems

Objective:

Coastal eutrophication that results from increased nutrient supply is a critical problem worldwide, causing major changes in marine populations and communities. The overall objective of this research project was to develop an indicator that quantifies nutrient supply to tropical and temperate marine ecosystems using the tissue nitrogen (N) and phosphorus (P) content of macroalgae. To complement the present suite of indicators used to measure eutrophication, this indicator is targeted to be especially useful in systems where nutrients are supplied in pulses or those where nonpoint sources of nutrients such as groundwater or fluxes from the benthos are important. The specific objectives of this research project were to: (1) identify and test potential species for use as indicators; (2) establish relationships between timing and magnitude of nutrient supply and accumulation of N and P in algal tissue; (3) establish quantitative relationships between environmental and ecological conditions, N and P supply, and tissue N and P and investigate the usefulness of 15N as an indicator of nutrient sources; and (4) field test the indicator in both temperate and tropical habitats.

Summary/Accomplishments (Outputs/Outcomes):

Objective 1: Identify Potential Species

We identified four species of macroalgae that make an ideal combination of indicators along the west coast of the United States. Each complements the other across this broad latitudinal range with its associated broad range in nutrient supply. Enteromorpha intestinalis is the best indicator species for southern California and in northern regions is replaced in usefulness by Ulva expansa in estuaries and Ulva lactuca on rocky shores. With these species, isotopic ratios of N, in conjunction with tissue N content, proved ideal to indicate both magnitude and source of N input. In areas of very high nutrient supply such as Puget Sound Porphyra perforata may be best; its habitat is high in the intertidal and therefore limited submergence time may keep tissues from being saturated under high nutrient loads. Our results demonstrate that Acanthophora spicifera is the best indicator species within tropical marine habitats. This species has open branches and upright morphologies that extend into the water column to “sample” nutrients. In contrast, Dictyota divaricata is not an effective indicator of water nutrient supply but may be useful for sediment sources or where advection is very important.

Objective 2: Verify Accumulation of N and P in Tissue

One criterion of an algal indicator of nutrient supply is the ability to accumulate N and P in tissues. We quantified this ability for the different species by conducting a series of identical experiments for each of the species in all study locations. Each experiment began with algae and water collected from a specific site. We conducted a 2 X 2 factorial experiment varying the amount of N and P in the water and measured accumulation of N and P in tissues.

Experiments were conducted in three tropical regions (Puerto Rico, Honduras, and the Eastern Tropical Pacific, HI) and three temperate regions (southern California, northern California, and Friday Harbor Labs, WA). From these experiments, we determined that all the target species identified in objective 1 were able to sequester N and P in response to nutrient N and P addition. Nutrient history of algae from different locations, however, is very important in determining the ability to sequester and store nutrients. Algae that are kept under low nutrient conditions have a greater ability to take up nutrients during nutrient pulses. From this, we determined that the algae used in indicator experiments should be preconditioned in nutrient-poor water prior to deployment.

Objective 3: Establish Quantitative Relationships Between Environmental and Ecological Conditions, N and P Supply, and Tissue N and P To Investigate 15N as a Potential Indicator

To be a useful indicator, a macroalga must be able to record nutrient supply in a quantitative way. This relationship must be predictable and reliable. The objective of this series of experiments was to develop these relationships and to determine if they varied in response to the variety of physical, chemical, and biological conditions that they may be subject to in the field. In addition, we studied the trophic relationships of these macroalgae to determine to what level we had to ensure the indicators were protected from herbivory. A final addition to this body of research was to investigate the usefulness of seagrass as a longer term integrator of nutrient supply, especially from the sediment.

Experiments on E. intestinalis and U. expansa quantified the relationship between the supply of N and P and accumulation in the tissue. The results identified the importance of using algae with initially low tissue nutrient content, of using total mass of N and P to remove the confounding effects of growth, and of ensuring at least a minimum of water motion during deployment. Our indicator alga E. intestinalis demonstrated the ability to take up NH4+, NO3-, and dissolved organic N simultaneously, a physiological adaptation that confers an advantage in estuarine waters with complex N sources, such as estuaries. Our experiments also demonstrated that 15N may be used as an indicator of N sources, as fractionation did not occur across a wide range of del 14N ratios (5-40) or over the concentration range of 50-500 µM NO3- or NH4+. Other experiments revealed that E. intestinalis has a rapid, quantifiable physiological response to increased nutrients across a wide range of environmental factors, including salinity, light, and nutrient source. This physiological adaptation to enhance uptake even during unfavorable conditions extends the usefulness of this species as an indicator, especially in habitats subject to extreme conditions.

Grazing studies outlined the importance of protecting indicators from herbivory during experimental deployment. Herbivory was strong across seagrass, mangrove, and coral reef habitats in tropical areas with intact fish populations. In overfished tropical areas, smaller invertebrate grazers replace large guilds; thus, the deployment protocol still requires protection by mesh cages for the indicators to function.

Experiments with seagrass showed that epiphytic algae had a rapid response to 15N additions, whereas seagrass blades took it up much more slowly. This suggests that algae and seagrass may be used in conjunction to measure nutrient supply across differing time scales.

Objective 4: Field Test Indicator

We conducted a large-scale field experiment in three estuaries in southern California to test our bioassay technique with E. intestinalis. We deployed the bioassays in both wet and dry seasons in 10 locations in each of the three estuaries to capture the estuarine gradient from head to mouth. The results show that the gradient in freshwater influence is only sometimes reflected as a nutrient gradient. Algal tissue N and P did not vary in a predictable manner based on either freshwater inflow or water column nutrient sampling at a snapshot in time. Tissue N in algae increased at all stations, in all estuaries, and in all seasons. This suggests that these systems are highly enriched year-round. In addition, 15N in algal tissue increased throughout the estuary, suggesting an enriched N source such as groundwater enters the entire estuary. We also conducted field tests of A. spicifera in Puerto Rico and Hawaii. In each case, the tissue N of this alga reflected known nutrient supplies. When we tried other species in Honduras the results were equivocal, demonstrating that Acanthophora was a more useful indicator.

Significant Findings

Temperate Marine Ecosystems

  • Four species of macroalgae were identified successfully and tested for use as indicators.
  • Between these four species, we can sample both open coast and estuarine environments across a wide geographical area and with an order of magnitude different nutrient supplies.

Tropical Marine Ecosystems

  • Three species or species groups of algae were identified successfully and tested for use as indicators.
  • Macroalgal morphology determined the effectiveness of each species for measuring different nutrient sources (benthic versus water column).

Indicator Methodology Development

  • Macroalgae must be cultured in low nutrient water prior to deployment to ensure that they “sample” the environment in a quantifiable, predictable manner.
  • Total N mass in deployed algae can be used to normalize algae with different growth rates across environmental gradients.
  • 15N accumulation in tissue in conjunction with N mass may be a very powerful tool for determining the source of N supply.


Journal Articles on this Report : 21 Displayed | Download in RIS Format

Other project views: All 50 publications 24 publications in selected types All 22 journal articles
Type Citation Project Document Sources
Journal Article Armitage AR, Fong P. Upward cascading effects of nutrients: shifts in a benthic microalgal community and a negative herbivore response. Oecologia 2004;139(4):560-567. R827637 (Final)
  • Abstract from PubMed
  • Full-text: ResearchGate - Abstract & Full Text PDF
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  • Abstract: Springer-Abstract
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  • Journal Article Armitage AR, Fong P. Gastropod colonization of a created coastal wetland: potential influences of habitat suitability and dispersal ability. Restoration Ecology 2004;12(3):391-400. R827637 (2000)
    R827637 (2001)
    R827637 (2002)
    R827637 (Final)
  • Full-text: EPA-Full Text PDF
  • Abstract: Wiley-Abstract
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  • Other: ResearchGate - Abstract & Full Text PDF
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  • Journal Article Boyer KE, Fong P, Vance RR, Ambrose RF. Salicornia virginica in a Southern California salt march: seasonal patterns and a nutrient-enrichment experiment. Wetlands 2001;21(3):315-326. R827637 (2002)
    R827637 (Final)
    R825381 (1999)
    R825381 (Final)
  • Full-text: San Francisco State University-Full Text PDF
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  • Abstract: BioOne-Abstract
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  • Journal Article Boyer KE, Fong P, Armitage AR, Cohen RA. Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 2004;23(4):530-538. R827637 (2002)
    R827637 (Final)
  • Full-text: San Francisco State University-Full Text PDF
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  • Abstract: Springer-Abstract
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  • Other: ResearchGate - Abstract & Full Text PDF
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  • Journal Article Boyer KE, Fong P. Macroalgal-mediated transfers of water column nitrogen to intertidal sediments and salt marsh plants. Journal of Experimental Marine Biology and Ecology 2005;321(1):59-69. R827637 (Final)
    R825381 (1999)
    R825381 (Final)
  • Full-text: ScienceDirect-Full Text PDF
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  • Abstract: ScienceDirect-Abstract & Full Text HTML
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  • Other: SFSU-Full Text PDF
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  • Journal Article Boyer KE, Fong P. Co-occurrence of habitat-modifying invertebrates: effects on structural and functional properties of a created salt marsh. Oecologia 2005;143(4):619-628. R827637 (Final)
    R825381 (1999)
    R825381 (Final)
  • Abstract from PubMed
  • Full-text: ResearchGate - Abstract & Full Text PDF
    Exit
  • Abstract: Springer-Abstract
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  • Journal Article Boyle KA, Kamer K, Fong P. Spatial and temporal patterns in sediment and water column nutrients in a eutrophic Southern California estuary. Estuaries and Coasts 2004;27(3):378-388. R827637 (2002)
    R827637 (Final)
    R825381 (1999)
    R825381 (Final)
  • Abstract: Springer-Abstract
    Exit
  • Journal Article Cohen RA, Fong P. Physiological responses of a bloom-forming green macroalga to short-term change in salinity, nutrients, and light help explain its ecological success. Estuaries and Coasts 2004;27(2):209-216. R827637 (2002)
    R827637 (Final)
  • Abstract: Springer-Abstract
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  • Journal Article Cohen RA, Fong P. Nitrogen uptake and assimilation in Enteromorpha intestinalis (L.) Link (Chlorophyta): using 15N to determine preference during simultaneous pulses of nitrate and ammonium. Journal of Experimental Marine Biology and Ecology 2004;309(1):67-77. R827637 (2000)
    R827637 (2001)
    R827637 (2002)
    R827637 (Final)
  • Full-text: ScienceDirect - Full Text HTML
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  • Abstract: ScienceDirect-Abstract
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  • Other: ScienceDirect - Full Text PDF
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  • Journal Article Cohen RA, Fong P. Experimental evidence supports the use of δ15N content of the opportunistic green macroalga Enteromorpha intestinalis (Chlorophyta) to determine nitrogen sources to estuaries. Journal of Phycology 2005;41(2):287-293. R827637 (Final)
  • Abstract: Wiley-Abstract
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  • Journal Article Cohen RA, Fong P. Using opportunistic green macroalgae as an indicator of anthropogenic influences in southern California estuaries. Ecological Applications 2006;16(4):1405-1420. R827637 (Final)
  • Abstract: ESA - Abstract
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  • Journal Article Fong P, Zedler JB. Sources, sinks, and fluxes of nutrients (N + P) in a small highly modified urban estuary in southern California. Urban Ecosystems 2000;4(2):125-144. R827637 (2000)
    R827637 (Final)
  • Abstract: Springer-Abstract
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  • Journal Article Fong P, Kamer K, Boyer KE, Boyle KA. Nutrient content of macroalgae with differing morphologies may indicate sources of nutrients for tropical marine systems. Marine Ecology Progress Series 2001;220:137-152. R827637 (2000)
    R827637 (2002)
    R827637 (Final)
  • Full-text: MEPS-Full Text PDF
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  • Abstract: MEPS-Abstract
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  • Other: ResearchGate - Full Text PDF
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  • Journal Article Fong P, Boyer KE, Kamer K, Boyle KA. Influence of initial tissue nutrient status of tropical marine algae on response to nitrogen and phosphorus additions. Marine Ecology Progress Series 2003;262:111-123. R827637 (Final)
  • Full-text: MEPS-Full Text PDF
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  • Abstract: MEPS-Abstract
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  • Other: ResearchGate - Full Text PDF
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  • Journal Article Fong P, Fong JJ, Fong CR. Growth, nutrient storage, and release of dissolved organic nitrogen by Enteromorpha intestinalis in response to pulses of nitrogen and phosphorus. Aquatic Botany 2004;78(1):83-95. R827637 (2002)
    R827637 (Final)
  • Full-text: ScienceDirect-Full Text PDF
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  • Abstract: ScienceDirect-Abstract & Full Text HTML
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  • Other: ResearchGate - Abstract & Full Text PDF
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  • Journal Article Kamer K, Fong P. A fluctuating salinity regime mitigates the negative effects of reduced salinity on the estuarine macroalga, Enteromorpha intestinalis (L.) link. Journal of Experimental Marine Biology and Ecology 2000;254(1):53-69. R827637 (2000)
    R827637 (Final)
    R825381 (1999)
    R825381 (Final)
  • Abstract from PubMed
  • Full-text: ScienceDirect - Full Text HTML
    Exit
  • Abstract: ScienceDirect-Abstract
    Exit
  • Other: ScienceDirect - Full Text PDF
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  • Journal Article Kamer K, Fong P. Nitrogen enrichment ameliorates the negative effects of reduced salinity on the green macroalga Enteromorpha intestinalis. Marine Ecology Progress Series 2001;218:87-93. R827637 (2000)
    R827637 (2002)
    R827637 (Final)
  • Full-text: MEPS-Full Text PDF
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  • Abstract: MEPS-Abstract
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  • Other: ResearchGate - Full Text PDF
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  • Journal Article Kamer K, Boyle KA, Fong P. Macroalgal bloom dynamics in a highly eutrophic southern California estuary. Estuaries and Coasts 2001;24(4):623-635. R827637 (2000)
    R827637 (2002)
    R827637 (Final)
    R825381 (1999)
    R825381 (Final)
  • Abstract: Springer-Abstract
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  • Journal Article Kamer K, Fong P, Kennison R, Schiff K. Nutrient limitation of the macroalga Enteromorpha intestinalis collected along a resource gradient in a highly eutrophic estuary. Estuaries and Coasts 2004;27(2):201-208. R827637 (2002)
    R827637 (Final)
  • Abstract: Springer-Abstract
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  • Journal Article Kamer K, Fong P, Kennison RL, Schiff K. 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. Aquatic Ecology 2004;38(1):45-56. R827637 (2000)
    R827637 (2001)
    R827637 (2002)
    R827637 (Final)
  • Abstract: Springer-Abstract
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  • Journal Article Smith JR, Reed BJ, Mohajerani L, Fong P. Influence of abiotic factors on the persistence of kelp habitats along the north coast of Santa Monica Bay. Southern California Academy of Sciences Bulletin 2004;103(2):79-92. R827637 (Final)
  • Full-text: SCASB-Full Text PDF
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  • Abstract: SCASB-Abstract
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  • Supplemental Keywords:

    algae, algal growth, aquatic ecosystem, bays, coastal ecosystem, coastal environments, ecological indicators, ecosystem indicators, effluent, environmental monitoring, estuaries, estuarine ecosystems, hydrological stability, macroalgae, marine ecosystem, nitrogen, N, nutrient supply, nutrient transport, phosphorus, P, risk assessment, stressors, tropical ecosystems,, RFA, Scientific Discipline, Geographic Area, Water, Ecosystem Protection/Environmental Exposure & Risk, Nutrients, Ecology, Ecosystem/Assessment/Indicators, Ecosystem Protection, State, Ecological Effects - Environmental Exposure & Risk, Ecology and Ecosystems, coastal ecosystem, aquatic ecosystem, environmental monitoring, hydrological stability, nutrient supply, nutrient transport, risk assessment, bays, marine ecosystem, algae, estuaries, stressors, macroalgae, tropical ecosystems, algal growth, coastal environments, Puerto Rico, effluent, ecosystem indicators, estuarine ecosystems, tropical storms, water quality, phosphorus, ecological indicators, California (CA), Florida, nitrogen

    Progress and Final Reports:

    Original Abstract
  • 2000 Progress Report
  • 2001 Progress Report