Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp.

Receiving coastal waters and estuaries are among the most nutrient-enriched environments on earth, and one of the symptoms of the resulting eutrophication is the proliferation of opportunistic, fast-growing marine seaweeds. Here, we used a widespread macroalga often involved in blooms, Ulva spp., to investigate how supply of nitrogen (N) and phosphorus (P), the two main potential growth-limiting nutrients, influence macroalgal growth in temperate and tropical coastal waters ranging from low- to high-nutrient supplies. We carried out N and P enrichment field experiments on Ulva spp. in seven coastal systems, with one of these systems represented by three different subestuaries, for a total of nine sites. We showed that rate of growth of Ulva spp. was directly correlated to annual dissolved inorganic nitrogen (DIN) concentrations, where growth increased with increasing DIN concentration. Internal N pools of macroalgal fronds were also linked to increased DIN supply, and algal growth rates were tightly coupled to these internal N pools. The increases in DIN appeared to be related to greater inputs of wastewater to these coastal waters as indicated by high δ15N signatures of the algae as DIN increased. N and P enrichment experiments showed that rate of macroalgal growth was controlled by supply of DIN where ambient DIN concentrations were low, and by P where DIN concentrations were higher, regardless of latitude or geographic setting. These results suggest that understanding the basis for macroalgal blooms, and management of these harmful phenomena, will require information as to nutrient sources, and actions to reduce supply of N and P in coastal waters concerned.

[1]  M. Piriz,et al.  Symptoms of Eutrophication in Intertidal Macroalgal Assemblages of Nuevo Gulf (Patagonia, Argentina) , 2002 .

[2]  E. Serviere-Zaragoza,et al.  Species composition and seasonal changes in macroalgal blooms in lagoons along the southeastern Gulf of California , 2008 .

[3]  Per Jonsson,et al.  MARINE EUTROPHICATION CASE-STUDIES IN SWEDEN , 1990 .

[4]  C. Hopkinson,et al.  Using stable isotopes to trace sewage-derived material through Boston Harbor and Massachusetts Bay , 1999 .

[5]  Flux of ammonium from surf-zone and nearshore sediments in Nahant Bay, Massachusetts, USA, in relation to free-living Pilayella littoralis , 1988 .

[6]  P. Wheeler,et al.  SEASONAL FLUCTUATIONS IN TISSUE NITROGEN, PHOSPHORUS, AND N:P FOR FIVE MACROALGAL SPECIES COMMON TO THE PACIFIC NORTHWEST COAST 1 , 1992 .

[7]  B. Lapointe,et al.  Macroalgal blooms on southeast Florida coral reefs: II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen , 2005 .

[8]  R. Rosenberg,et al.  Effects of eutrophication on benthic communities including fish: Swedish west coast , 1990 .

[9]  B. Lapointe,et al.  Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen sources , 2004 .

[10]  B. Lapointe,et al.  Nutrient-enhanced growth of Cladophora prolifera in harrington sound, bermuda: Eutrophication of a confined, phosphorus-limited marine ecosystem , 1989 .

[11]  P. Morand,et al.  Macroalgal Population and Sustainability , 2005 .

[12]  B. K. Sullivan,et al.  NUTRIENTS AND THE PRODUCTIVITY OF ESTUARINE AND COASTAL MARINE ECOSYSTEMS , 1986 .

[13]  L. Pihl,et al.  Effects of filamentous green algal mats on benthic macrofaunal functional feeding groups , 2001 .

[14]  M. Carrer,et al.  Loss, growth and transport dynamics of Chaetomorpha aerea and Ulva rigida in the Lagoon of Venice during an early summer field campaign , 1997 .

[15]  D. Schindler,et al.  Eutrophication science: where do we go from here? , 2009, Trends in ecology & evolution.

[16]  William J. Kimmerer,et al.  Kaneohe Bay Sewage Diversion Experiment: Perspectives on Ecosystem Responses to Nutritional Perturbation , 1981 .

[17]  H. Lotze,et al.  Propagule banks, herbivory and nutrient supply control population development and dominance patterns in macroalgal blooms , 2000 .

[18]  I. Valiela,et al.  Using δ15N to Assess Coupling between Watersheds and Estuaries in Temperate and Tropical Regions , 2008 .

[19]  A. J. Smit,et al.  Use of δ15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal , 2002 .

[20]  R. Howarth,et al.  Variable rates of phosphate uptake by shallow marine carbonate sediments: Mechanisms and ecological significance , 1994 .

[21]  B. Lapointe,et al.  Nutrient availability to marine macroalgae in siliciclastic versus carbonate-rich coastal waters , 1992 .

[22]  A. Sfriso,et al.  Macrofauna impact on Ulva rigida C. Ag. production and relationship with environmental variables in the lagoon of Venice. , 2001, Marine environmental research.

[23]  P. Doering,et al.  An ecosystem level experiment on nutrient limitation in temperate coastal marine environments , 1995 .

[24]  R. Howarth Coastal nitrogen pollution: A review of sources and trends globally and regionally , 2008 .

[25]  M. Pedersen,et al.  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. , 1996 .

[26]  A. Whitfield Coastal Lagoons – Critical Habitats of Environmental Change , 2011 .

[27]  S. Nixon,et al.  Natural and anthropogenic nitrogen uptake by bloom-forming macroalgae. , 2008, Marine pollution bulletin.

[28]  P. Wheeler,et al.  EFFECT OF NITROGEN AND PHOSPHORUS SUPPLY ON GROWTH AND TISSUE COMPOSITION OF ULVA FENESTRATA AND ENTEROMORPHA INTESTINALIS (ULVALES, CHLOROPHYTA) 1 , 1990 .

[29]  M. Maldonado,et al.  Growth, nutrient uptake capacities and tissue constituents of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae related to site-specific nitrogen loading rates , 1994 .

[30]  I. Valiela,et al.  Linking nitrogen in estuarine producers to land‐derived sources , 1998 .

[31]  M. Voss,et al.  Anthropogenic nitrogen input traced by means of delta15N values in macroalgae: results from in-situ incubation experiments. , 2006, The Science of the total environment.

[32]  Kathleen Segerson,et al.  Clean Coastal Waters - Understanding and Reducing the Effects of Nutrient Pollution , 2000 .

[33]  R. Díaz Overview of hypoxia around the world. , 2001, Journal of environmental quality.

[34]  P. Fong,et al.  Nutrient content of macroalgae with differing morphologies may indicate sources of nutrients for tropical marine systems , 2001 .

[35]  S. Larned,et al.  Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae , 1998 .

[36]  Qianguo Xing,et al.  World's largest macroalgal bloom caused by expansion of seaweed aquaculture in China. , 2009, Marine pollution bulletin.

[37]  Y. Olsen,et al.  Restructuring of benthic communities in eutrophic estuaries: Lower abundance of prey leads to trophic shifts from omnivory to grazing , 2009 .

[38]  I. Valiela,et al.  Controls Acting on Benthic Macrophyte Communities in a Temperate and a Tropical Estuary , 2010 .

[39]  K. Lajtha,et al.  Couplings of watersheds and coastal waters: Sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts , 1992 .

[40]  K. Boicourt,et al.  Effects of nutrient enrichment in the nation's estuaries: A decade of change , 2008 .

[41]  James L. McClelland,et al.  Use of isotopic signatures to assess the food web in a tropical shallow marine ecosystem of Southeastern Brazil , 2006, Aquatic Ecology.

[42]  P. Lavery,et al.  Changes in the biomass and species composition of macroalgae in a eutrophic estuary , 1991 .

[43]  João Carlos Marques,et al.  Hydrodynamics as a Major Factor Controlling the Occurrence of Green Macroalgal Blooms in a Eutrophic Estuary: A Case Study on the Influence of Precipitation and River Management , 2001 .

[44]  Antonio Marcomini,et al.  Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice , 1992 .

[45]  J. Hauxwell,et al.  Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences , 1997 .

[46]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[47]  D. Raffaelli,et al.  Ecological impact of green macroalgal blooms , 1998 .

[48]  S. Nixon,et al.  Chapter 16 – NITROGEN IN ESTUARINE AND COASTAL MARINE ECOSYSTEMS , 1983 .

[49]  R. Pruell,et al.  Nitrogen isotope ratios in estuarine biota collected along a nutrient gradient in Narragansett Bay, Rhode Island, USA. , 2006, Marine Pollution Bulletin.

[50]  Peter J. Barile,et al.  Evidence of Anthropogenic Nitrogen Enrichment of the Littoral Waters of East Central Florida , 2004 .

[51]  Dongyan Liu,et al.  The Impact of Sewage Discharge on the Macroalgae Community in the Yellow Sea Coastal Area Around Qingdao, China , 2007 .

[52]  Paul C. Silva,et al.  Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera , 2003 .

[53]  D. E. Roberts,et al.  Effects of the green macroalga Enteromorpha intestinalis on macrobenthic and seagrass assemblages in a shallow coastal estuary , 2004 .

[54]  R. Elmgren,et al.  MACROALGAL (FUCUS VESICULOSUS) δ15N VALUES TRACE DECREASE IN SEWAGE INFLUENCE , 2004 .

[55]  H. Lotze,et al.  Marine diversity shift linked to interactions among grazers, nutrients and propagule banks , 1999 .

[56]  James L. McClelland,et al.  Left running head: Fox et al. Right running head: Effects of nitrogen loads on macrophytes Macrophyte abundance in Waquoit Bay: Effects of land-derived nitrogen loads on seasonal and multi-year biomass patterns , 2008 .

[57]  E. Barbarino,et al.  Seasonal variations in tissue nitrogen and phosphorus of eight macroalgae from a tropical hypersaline coastal environment , 2005 .

[58]  K. McGlathery,et al.  Macroalgal distribution patterns in a shallow, soft-bottom lagoon, with emphasis on the nonnativeGracilaria vermiculophylla andCodium fragile , 2006 .

[59]  I. Valiela Global Coastal Change , 2006 .

[60]  Y. Olsen,et al.  Macroalgal responses to experimental nutrient enrichment in shallow coastal waters : growth, internal nutrient pools, and isotopic signatures , 2008 .

[61]  C. D’Avanzo,et al.  Ecosystem production and respiration in response to eutrophication in shallow temperate estuaries , 1996 .

[62]  M. Okada,et al.  Effects of ulvoid (Ulva spp.) accumulation on the structure and function of eelgrass (Zostera marina L.) bed. , 2007, Marine pollution bulletin.

[63]  P. Fong,et al.  Influence of initial tissue nutrient status of tropical marine algae on response to nitrogen and phosphorus additions , 2003 .

[64]  C. Hopkinson,et al.  Issues in ecology: Nutrient pollution of coastal rivers, bays, and seas , 2000 .

[65]  D. Raffaelli,et al.  Dynamic changes in seagrass assemblages under eutrophication and implications for recovery , 2004 .

[66]  C. Rostagno,et al.  Changes in biomass and botanical composition of beach-cast seaweeds in a disturbed coastal area from Argentine Patagonia , 2004, Journal of Applied Phycology.

[67]  P. Fong,et al.  Macroalgal bloom dynamics in a highly eutrophic southern California estuary , 2001 .

[68]  J. Hauxwell,et al.  MACROALGAL CANOPIES CONTRIBUTE TO EELGRASS (ZOSTERA MARINA) DECLINE IN TEMPERATE ESTUARINE ECOSYSTEMS , 2001 .

[69]  M. Pardal,et al.  Significant variations in the productivity of green macroalgae in a mesotidal estuary: implications to the nutrient loading of the system and the adjacent coastal area. , 2007, Marine pollution bulletin.

[70]  J. Zedler,et al.  Salinity stress, nitrogen competition, and facilitation: what controls seasonal succession of two opportunistic green macroalgae? , 1996 .

[71]  Carlos M. Duarte,et al.  Submerged aquatic vegetation in relation to different nutrient regimes , 1995 .

[72]  I. Valiela,et al.  Nitrate reductase and glutamine synthetase activity, internal N pools, and growth of Ulva lactuca: responses to long and short-term N supply , 2007 .

[73]  I. Valiela,et al.  Macrophytes as indicators of land‐derived wastewater: Application of a δ15N method in aquatic systems , 2005 .

[74]  R. Fujita The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae , 1985 .

[75]  J. Carballo,et al.  Qualitative Changes in Macroalgal Assemblages under Two Contrasting Climatic Conditions in a Subtropical Estuary , 2002 .

[76]  A. Marcomini,et al.  Macrophyte production in a shallow coastal lagoon. Part I: Coupling with chemico-physical parameters and nutrient concentrations in waters , 1997 .

[77]  João Carlos Marques,et al.  Management of a shallow temperate estuary to control eutrophication: The effect of hydrodynamics on the system’s nutrient loading , 2005 .

[78]  C. Schneider,et al.  The life history and morphology of free-living Pilayella littoralis (L.) Kjellm. (Ectocarpaceae, Ectocarpales) in Nahant Bay, Massachusetts , 1982 .