Effects of the decomposing green macroalga Ulva (Enteromorpha) prolifera on the growth of four red-tide species

The green macroalga Ulva (Enteromorpha) prolifera formed large-scale blooms (the so-called "green tide") from 2007 to 2010 in the Yellow Sea, China. In June 2008, huge amounts of floating U. prolifera accumulated along the coast of Qingdao. At the late stage of the green tide, a large amount of green algae sank to the bottom and decomposed, which led to concerns about derivative ecological and environmental problems, such as red tides. The effects of nutrient recycling from decomposing green tides on the growth of four selected red-tide causative species, i.e. Heterosigrna akashiwo, Alexandrium tamarense, Prorocentrum donghaiense and Skeletonema costatum, were studied in the laboratory. It was found that the decomposing green algae released considerable amounts of ammonium and phosphate into the surrounding seawater. The addition of effluent from the decomposing green algae promoted the rapid proliferation of the raphidophyte H. akashiwo, but inhibited the growth of the diatom S. costatum. The growth of two dinoflagellate species A. tamarense and P. donghaiense was triggered by the addition of low-concentration decomposing algal effluent, but inhibited by the high-concentration decomposing algal effluent, probably due to toxicity from high concentrations of ammonium or water-soluble allelochemicals present in the decomposing effluent. We conclude that the decomposition of green algae releases inorganic nutrients, particularly ammonium, into seawater where the nutrients could support red tides once they were taken up by the opportunistic microalgae. (C) 2012 Elsevier B.V. All rights reserved.

[1]  S. Dong,et al.  Allelopathic growth inhibition of Prorocentrum micans (Dinophyta) by Ulva pertusa and Ulva linza (Chlorophyta) in laboratory cultures , 2005 .

[2]  B. Lapointe,et al.  Drift rhodophyte blooms emerge in Lee County, Florida, USA : Evidence of escalating coastal eutrophication , 2007 .

[3]  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 .

[4]  T. Blackburn,et al.  Nutrient fluxes and growth of Cladophora sericea in a shallow Danish bay , 1993 .

[5]  G. Yoshida,et al.  Crossing test among floating Ulva thalli forming ‘green tide’ in Japan , 2004 .

[6]  P. Harrison,et al.  Ratio of nitrogen to phosphorus in the Pearl River and effects on the estuarine coastal waters: Nutrient management strategy in Hong Kong , 2011 .

[7]  Martha N. Jones Nitrate reduction by shaking with cadmium: Alternative to cadmium columns , 1984 .

[8]  Song Sun,et al.  Tracking the algal origin of the Ulva bloom in the Yellow Sea by a combination of molecular, morphological and physiological analyses. , 2010, Marine environmental research.

[9]  S. Qin,et al.  Molecular phylogenetic analysis of attached Ulvaceae species and free-floating Enteromorpha from Qingdao coasts in 2007 , 2008 .

[10]  D. Anderson,et al.  Manual on Harmful Marine Microalgae, IOC Manuals and Guides No. 33 , 1995 .

[11]  M. Stanhope,et al.  Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. , 2002, American journal of botany.

[12]  D. Franz,et al.  Effects of a macroalgal mat (Ulva lactuca) on estuarine sand flat copepods: an experimental study , 2002 .

[13]  P. Birch,et al.  Decomposition of Cladophora II. In vitro Studies of Nitrogen and Phosphorus Regeneration , 1983 .

[14]  S. Dong,et al.  Comparative studies on the allelopathic effects of two different strains of Ulva pertusa on Heterosigma akashiwo and Alexandrium tamarense , 2003 .

[15]  K. Sand‐Jensen,et al.  Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries , 1991 .

[16]  M. Flindt,et al.  Nutrient cycling and plant dynamics in estuaries: A brief review , 1999 .

[17]  R. L. Fletcher The Occurrence of “Green Tides”— a Review , 1996 .

[18]  Donald M. Anderson,et al.  Bloom dynamics of toxic Alexandrium species in the northeastern U.S , 1997 .

[19]  C. Tomas,et al.  Identifying marine phytoplankton , 1997 .

[20]  D. Anderson,et al.  Biogeography of toxic dinoflagellates in the genusAlexandrium from the northeastern United States and Canada , 1994 .

[21]  S. Taguchi,et al.  Response of the dinoflagellate Alexandrium tamarense to a range of nitrogen sources and concentrations: growth rate, chemical carbon and nitrogen, and pigments , 2004, Hydrobiologia.

[22]  A. Marcomini,et al.  Species composition, biomass, and net primary production in shallow coastal waters: the Venice lagoon , 1993 .

[23]  L. Song-hui Effects of different inorganic nitrogen sources on the growth of Prorocentrum donghaiense , 2006 .

[24]  J. L. Pérez-Lloréns,et al.  BIOMASS AND DYNAMICS OF GROWTH OF ULVA SPECIES IN PALMONES RIVER ESTUARY 1 , 1997 .

[25]  W. Cochlan,et al.  Nitrogen utilization by the raphidophyte Heterosigma akashiwo: Growth and uptake kinetics in laboratory cultures , 2007 .

[26]  D. Thornton,et al.  Effect of temperature on the aggregation of Skeletonema costatum (Bacillariophyceae) and the implication for carbon flux in coastal waters , 1998 .

[27]  G. Wolfe,et al.  Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage , 2001 .

[28]  L. Yan,et al.  A Preliminary Study on Phytoplankton Community Structure and Its Changes in the Jiaozhou Bay , 2005 .

[29]  Charles S. Yentsch,et al.  Anatomy of a red tide bloom off the southwest coast of Florida , 2008 .

[30]  MACROPHYTE COMMUNITIES AND THEIR IMPACT ON BENTHIC FLUXES OF OXYGEN, SULPHIDE AND NUTRIENTS IN SHALLOW EUTROPHIC ENVIRONMENTS , 1996 .

[31]  P. H. Nienhuis,et al.  Marine Benthic Vegetation , 1996, Ecological Studies.

[32]  M. Trimmer,et al.  Seasonal organic mineralisation and denitrification in intertidal sediments and their relationship to the abundance of Enteromorpha sp. and Ulva sp. , 2000 .

[33]  Guangqiang Zhao,et al.  Allelopathic effects of Ulva lactuca on selected species of harmful bloom-forming microalgae in laboratory cultures , 2008 .

[34]  Yunyan Deng,et al.  The possibility analysis of habitats, origin and reappearance of bloom green alga (Enteromorpha prolifera) on inshore of western Yellow Sea , 2009 .

[35]  X. Briand,et al.  Excessive Growth of Macroalgae: A Symptom of Environmental Disturbance , 1996 .

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

[37]  Gustaaf M. Hallegraeff,et al.  Harmful algal blooms: a global overview , 1995 .

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

[39]  Guangqiang Zhao,et al.  Allelopathic interactions between the macroalga Ulva pertusa and eight microalgal species , 2004 .

[40]  P. Viaroli,et al.  Benthic decomposition of Zostera marina roots: a controlled laboratory experiment , 2004 .

[41]  T. Nelson,et al.  ARE “GREEN TIDES” HARMFUL ALGAL BLOOMS? TOXIC PROPERTIES OF WATER‐SOLUBLE EXTRACTS FROM TWO BLOOM‐FORMING MACROALGAE, ULVA FENESTRATA AND ULVARIA OBSCURA (ULVOPHYCEAE) , 2003 .

[42]  K. Furuya,et al.  Species-specific productivity of Skeletonema costatum(Bacillariophyceae)in the inner part of Tokyo Bay. , 1991 .

[43]  T. Nelson,et al.  A manipulative experiment demonstrates that blooms of the macroalga Ulvaria obscura can reduce eelgrass shoot density , 2001 .

[44]  B. Lapointe,et al.  Macroalgal blooms on southeast Florida coral reefs I. Nutrient stoichiometry of the invasive green alga Codium isthmocladum in the wider Caribbean indicates nutrient enrichment , 2005 .

[45]  E. Pieczyńska,et al.  Effect of decomposing filamentous algae on the growth of Elodea canadensis Michx. (a laboratory experiment) , 1996 .

[46]  Z. Mohamed Allelopathic activity of Spirogyra sp.: stimulating bloom formation and toxin production by Oscillatoria agardhii in some irrigation canals, Egypt , 2002 .

[47]  J. Rivers,et al.  Physiological responses of the opportunistic macroalgae Cladophora vagabunda (L.) van den Hoek and Gracilaria tikvahiae (McLachlan) to environmental disturbances associated with eutrophication , 1995 .

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

[49]  K. McGlathery MACROALGAL BLOOMS CONTRIBUTE TO THE DECLINE OF SEAGRASS IN NUTRIENT‐ENRICHED COASTAL WATERS , 2001 .

[50]  D. Anderson,et al.  Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae) 1 , 2007 .

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

[52]  Agata Tarmanowska Laboratory studies on the influence of living and decomposing filamentous algae on the growth of Elodea canadensis Michx , 1995 .