Review of the brown tides caused by Aureococcus anophagefferens
QIAO Ling1,2,3, ZHEN Yu1,2,3, MI Tie-Zhu1,2,3
1. Key Laboratory of Marine Environment and Ecology, Ministry of Education, Qingdao 266100, China;
2. College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China;
3. Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
Abstract:The brown tides caused by Aureococcus anophagefferens firstly broke out in some coastal embayments of the northeastern United States in 1985.Subsequently, in 1997, A.anophagefferens blooms occurred in Saldanha Bay, South Africa.In 2009, the same bloom was reported in Qinhuangdao, China, making China the third country influenced by A.anophagefferens brown tide.Although A.anophagefferens have no direct, negative effects on human health, they can stunt or poison shellfish, resulting in significant economic losses and serious ecological damage.In this paper it is reviewed that the research advances in physiological and biochemical characteristics, the reasons of outbreak and demise, ecological consequences, and prevention measures of A.anophagefferens, which will provide scientific basis for preventing brown tides and maintaining marine ecosystem stability.
HAMMANN S,TILLMANN U,SCHRÖDERA M,et al.Profiling the fatty acids from a strain of the microalgae Alexandrium tamarense by means of high-speed counter-current chromatography and gas chromatography coupled with mass spectrometry[J].Journal of Chromatography A,2013,1312:93-103.
[3]
许艳婷.赤潮赤潮异弯藻培养液CDOM分析及其潜在的化感作用[D].宁波:宁波大学,2011.
[4]
CHAPMAN M G,UNDERWOOD A J.Evaluation of ecological engineering of "armoured" shorelines to improve their value as habitat[J].Journal of Experimental Marine Biology and Ecology,2011,400(1/2):302-313.
[5]
GOBLER C J,SAÑUDO-WILHELMY S A.Temporal variability of groundwater seepage and brown tide blooms in a Long Island embayment[J].Marine Ecology Progress Series,2001,217:299-309.
[6]
Hester A S, Mcdonald J S. Natural gas hydrocarbons for petrochemicals[J]. Industrial & Engineering Chemistry, 1956, 48(2):168-177
[7]
MAHROUS E A,FARAG M A.Two dimensional NMR spectroscopic approaches for exploring plant metabolome:A review[J].Journal of Advanced Research,2015,6(1):3-15.
[8]
HARTIG J H,ZARULL M A,COOK A.Soft shoreline engineering survey of ecological effectiveness[J].Ecological Engineering,2011,37(8):1231-1238.
[9]
GOBLER C J,SUNDA W G.Ecosystem disruptive algal blooms of the brown tide species,Aureococcus anophagefferens and Aureoumbra lagunensis [J].Harmful Algae,2012,14:36-45.
ALAMSJAH M A,HIRAO S,ISHIBASHI F,et al.Isolation and structure determination of algicidal compounds from Ulva fasciata[J].Bioscience,Biotechnology, and Biochemistry,2005,69(11):2186-2192.
[13]
VANDENBRUWAENE W,MEIRE P,TEMMERMAN S.Formation and evolution of a tidal channel network within a constructed tidal marsh[J].Geomorphology,2012,151-152:114-125.
[14]
GOBLER C J,BERRY D L,DYHRMAN S T,et al.Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics[J].Proceedings of the National Academy of Sciences,2011,108(11):4352-4357.
[15]
Talu O. Needs, status, techniques and problems with binary gas adsorption experiments[J]. Advances in Colloid and Interface Science, 1998, 76:227-269
[16]
ETCHEGARAY A,RABELLO E,DIECKMANN R,et al.Algicide production by the filamentous cyanobacterium Fischerellasp.CENA 19[J].Journal of Applied Phycology,2004, 16(3):237-243.
ROMAN C T,NIERING W A,WARREN R S.Salt marsh vegetation change in response to tidal restriction[J].Environmental Management,1984,8(2):141-149.
[19]
BERG G M,SHRAGER J,GLÖCKNER G,et al.Understanding nitrogen limitation in Aureococcus anophagefferens (Pelagophyceae) through cDNA and qRT-PCR analysis[J].Journal of Phycology,2008,44(5):1235-1249.
[20]
Balilehvand S, Hashemianazdeh S M,Razavi S, et al. Investigation of hydrogen and methane adsorption/separation on silicon nanotubes:A hierarchical multi-scale method from quantum mechanics to molecular simulation[J]. Adsorption, 2012, 18(1):13-22
[21]
LU H M,XIE H H,GONG Y X,et al.Secondary metabolites from the seaweed Gracilaria lemaneiformis and their allelopathic effects on Skeletonema costatum[J].Biochemical Systematics and Ecology,2011,39(4/5/6):397-400.
VAN PROOSDIJ D,LUNDHOLM J,NEATT N,et al.Ecological re-engineering of a freshwater impoundment for salt marsh restoration in a hypertidal system[J].Ecological Engineering,2010,36(10):1314-1332.
[25]
WURCH L L,HALEY S T,ORCHARD E D,et al.Nutrient-regulated transcriptional responses in the brown tide-forming alga Aureococcus anophagefferens [J].Environmental Microbiology,2011,13(2):468-481.
Zhou L, Wu J, Li M, et al. Prediction of multicomponent adsorption equilibrium of gas mixtures including supercritical components[J]. Chemical Engineering Science, 2005, 60(11):2 833-2 844
[28]
MA H Y,KROCK B,TILLMANN U,et al.Isolation of activity and partial characterization of large non-proteinaceous lytic allelochemicals produced by the marine dinoflagellate Alexandrium tamarense[J].Harmful Algae,2011,11:65-72.
[29]
HAINES P.Hydrological modelling of tidal re-inundation of an estuarine wetland in south-eastern Australia[J].Ecological Engineering,2013,52:79-87.
[30]
GLIBERT P M,MAGNIEN R,LOMAS M W,et al.Harmful algal blooms in the Chesapeake and Coastal Bays of Maryland,USA:Comparison of 1997,1998,and 1999 events[J].Estuaries,2001,24(6):875-883.
[31]
Bazan R, Bastos-Neto M, Staudt R, et al. Adsorption equilibria of natural gas components on activated carbon:Pure and mixed gas isotherms[J]. Adsorption Science & Technology, 2008, 26(5):323-332
[32]
YAMASAKI Y,OHMICHI Y,HIROSE M,et al.Low molecular weight allelochemicals produced by the diatom,Skeletonema costatum[J].Thalassas,2012,28(1):9-17.
[33]
BROOMES W,SENECA E D,WOODHOUSE JR W W.Tidal salt marsh restoration[J].Aquatic Botany,1988,32(1/2):1-22.
[34]
DOBLIN M A,POPELS L C,COYNE K J,et al.Transport of the harmful bloom alga Aureococcus anophagefferens by oceangoing ships and coastal boats[J].Applied and Environmental Microbiology,2004,70(11):6495-6500.
[35]
Zhou L, Bai S, Su W, et al. Comparative study of the excess versus absolute adsorption of CO2 on super activated carbon for the near-critical region[J]. Langmuir, 2003, 19 (7):2 683-2 690
[36]
PRINCE E K,POULSON K L,MYERS T L,et al.Characterization of allelopathic compounds from the red tide dinoflagellate Karenia brevis[J].Harmful Algae,2010,10(1):39-48.
[37]
张议文.海洋常见赤潮硅藻间的他感作用及他感物质研究[D].青岛:中国海洋大学,2014.
[38]
TEALJ M,WEINSTEIN M P.Ecological engineering,design,and construction considerations for marsh restorations in Delaware Bay,USA[J].Ecological Engineering,2002,18(5):607-618.
[39]
Plum Island Ecosystems LTER.The Long Term Ecological Research Network[EB/OL].2014,http://www.lternet.edu/sites/pie.
[40]
ADAM P.Saltmarsh ecology[M].Cambridge,New York:Cambridge University Press,1990.
[41]
GOBLER C J,RENAGHAN M J,BUCK N J.Impacts of nutrients and grazing mortality on the abundance of Aureococcus anophagefferens during a New York brown tide bloom[J].Limnology and Oceanography,2002,47(1):129-141.
[42]
Ryu Z, Zheng J, Wang M, et al. Characterization of pore size distributions on carbonaceous adsorbents by DFT[J]. Carbon, 1999, 37 (8):1 257-1 264
[43]
VANDANJON L,JAOUEN P,ROSSIGNOL N,et al.Concentration and desalting by membrane processes of a natural pigment produced by the marine diatom Haslea ostrearia Simonsen[J].Progress in Industrial Microbiology,1999,35:393-402.
[44]
LANGMAN O C,HALE J A,CORMACK C D,et al.Developing multimetric indices for monitoring ecological restoration progress in salt marshes[J].Marine Pollution Bulletin,2012,64(4):820-835.
[45]
NUZZI R,WATERS R M.Long-term perspective on the dynamics of brown tide blooms in Long Island coastal bays[J].Harmful Algae,2004,3(4):279-293.
[46]
Centeno T, Stoeckli F. The assessment of surface areas in porous carbons by two model-independent techniques, the DR equation and DFT[J]. Carbon, 2010, 48(9):2 478-2 486
[47]
孔祥明, 杨颖, 沈文龙, 等. CO2/CH4/N2在沸石13X-APG上的吸附平衡[J]. 化工学报, 2013, 64(8):2 117-2 124 Kong Xiangming, Yang Ying, Shen Wenlong, et al. Adsorption equilibrium of CO2, CH4 and N2 on zeolite 13X-APG[J]. CIESC Journal, 2013, 64(8):2 117-2 124(in Chinese)
[48]
POUVREAU J B,MORANÇAIS M,FLEURENCE J,et al.Method for the quantification of the blue-green pigment "marennine" synthesized by the marine diatom Haslea ostrearia (Gaillon/Bory) Simonsen using HPLC gel-filtration and photodiode-array detection[J].Journal of Applied Phycology,2007,19(3):263-270.
[49]
IRVINGA D,CONNELL S D,RUSSELL B D.Restoring coastal plants to improve global carbon storage:reaping what we sow[J].PLoS One,2011,6(3):1-6.
[50]
MACINTYRE H L,LOMAS M W,Cornwell J,et al.Mediation of benthic-pelagic coupling by microphytobenthos:an energy- and material-based model for initiation of blooms of Aureococcus anophagefferens [J].Harmful Algae,2004,3(4):403-437.
[51]
WINDARTO E,PRASETIYA F S,MOUGET J L,et al.Allelopathy effect of the blue diatom HasleaOstrearia (Gaillon) Simonsen:growth inhibition in aquaculture relevant microalgae[J].International Journal of Marine and Aquatic Resource Conservatian and Co-existence,2014,1(1):19-26.
[52]
CHMURA G L.What do we need to assess the sustainability of the tidal salt marsh carbon sink?[J].Ocean & Coastal Management,2013,83:25-31.
[53]
LOMAS M W,GILBERT P M,CLOUGHERTY D A,et al.Elevated organic nutrient ratios associated with brown tide algal blooms of Aureococcus anophagefferens (Pelagophyceae)[J].Journal of Plankton Research,2001,23(12):1339-1344.
[54]
LOMAS M W.Does urea-carbon contribute significantly to Aureococcus anophagefferens carbon nutrition[C]//Proceedings of the 10th International HAB Meeting,St.Petersburg,Florida,2003:402-404.
[55]
SUN Y Y,XU S Z,LI W H,et al.Antialgal substances from Isochrysis galbana and its effects on the growth of Isochrysis galbana and six species of feed microalgae[M]//ZHU E G,SAMBATH S.Information Technology and Agricultural Engineering.Berlin Heidelberg:Springer,2012,134:211-223.
ROBERTSONM M.Emerging ecosystem service markets:trends in a decade of entrepreneurial wetland banking[J].Frontiers in Ecology and the Environment,2006,4(6):297-302.
[58]
PUSTIZZI F,MACINTYRE H,WARNER M E,et al.Interaction of nitrogen source and light intensity on the growth and photosynthesis of the brown tide alga Aureococcus anophagefferens [J].Harmful Algae,2004,3(4):343-360.
[59]
POPLES L C,MACINTYRE H L,WARNER M E,et al.Physiological responses during dark survival and recovery in Aureococcus anophagefferens (Pelagophyceae)[J].Journal of Phycology,2007,43(1):32-42.
[60]
ONG H C,WILHELM S W,GOBLER C J,et al.Analyses of the complete chloroplast genome sequences of two members of the Pelagophyceae Aureococcus anophagefferens CCMP 1984 and Aureoumbra lagunensis CCMP 1507[J].Journal of Phycology,2010,46(3):602-615.
[61]
MULHOLLAND M R,BONEILLO G,MINOR E C.A comparison of N and C uptake during brown tide (Aureococcus anophagefferens) blooms from two coastal bays on the east coast of the USA[J].Harmful Algae,2004,3(4):361-376.
[62]
LOMAS M W,KANA T M,MACINTYRE H L,et al.Interannual variability of Aureococcus anophagefferens in Quantuck Bay,Long Island:natural test of the DON hypothesis[J].Harmful Algae,2004,3(4):389-402.
[63]
SIERACKI M E,KELLER M D,CUCCI T L,et al.Plankton community ecology during the bloom initiation period of the brown tide organism Aureococcus anophagefferens in coastal embayments of Long Island,N.Y.[Z].EOS Trans Am Geophys Union,1999,80:285.
[64]
ROBBINS H M,BRICELJ V M,WARD J E.In vivo effects of brown tide on the feeding function of the gill of the northern quahog Mercenaria mercenaria (Bivalvia:Veneridae)[J].Biology Bulletin,2010,219(1):61-71.
[65]
BRICELJ V M,MACQUARRIE S P,SCHAFFNER R A.Differential effects of Aureococcus anophagefferens isolates ("brown tide") in unialgal and mixed suspensions on bivalve feeding[J].Marine Biology,2001,139(4):605-616.
[66]
CERRATO R M,CARON D A,LONSDALE D J,et al.Effect of the northern quahog Mercenaria mercenaria on the development of blooms of the brown tide alga Aureococcus anophagefferens [J].Marine Ecology Progress Series,2004,281:93-108.
[67]
CARON D A,GOBLER C J,LONSDALE D J,et al.Microbial herbivory on the brown tide alga,Aureococcus anophagefferens:Results from natural ecosystems,mesocosms and laboratory experiments[J].Harmful Algae,2004,3(4):439-457.
[68]
GASTRICH M D,ANDERSON O R,COSPER E M.Viral-like particles (VLPS) in the alga,Aureococcus anophagefferens (pelagophyceae),during 1999-2000 brown tide blooms in Little Egg Harbor,New Jersey[J].Estuaries,2002,25(5):938-943.
[69]
GOBLER C J,ANDERSON O R,GASTRICH M D,et al.Ecological aspects of viral infection and lysis in the harmful brown tide alga Aureococcus anophagefferens [J].Aquatic Microbial Ecology,2007,47(1):25-36.
[70]
GASTRICH M D,LEIGH-BELL J A,GOBLER C J,et al.Viruses as potential regulators of regional brown tide blooms caused by the alga,Aureococcus anophagefferens [J].Estuaries,2004,27(1):112-119.
CAIOLA M G,PELLEGRINI S.Lysis of Microcystis aeruginosa (Kütz.) by Bdellovibrio-like bacteria[J].Journal of Phycology,1984,20(4):471-475.
[74]
FRAZIER A D,ROWE J M,RENTZ C A,et al.Bacterial lysis of Aureococcus anophagefferens CCMP 1784 (Pelagophyceae)[J].Journal of Phycology,2007,43(3):461-465.
TALMAGE S C,GOBLER C J.Effects of CO2 and the harmful alga Aureococcus anophagefferens on growth and survival of oyster and scallop larvae[J].Marine Ecology Progress Series,2012,464:121-134.
[79]
LONSDALE D J,COSPER E M,KIM W S,et al.Food web interactions in the plankton of Long Island bays,with preliminary observations on brown tide effects[J].Marine Ecology Progress Series,1996,134(1/2/3):247-263.
[80]
BAILEY J C,ANDERSEN R A.Analysis of clonal cultures of the brown tide algae Aureococcus and Aureoumbra (Pelagophyceae) using 18S rRNA,rbcL,and rubisco spacer sequences[J].Journal of Phycology,1999,35(3):570-574.
[81]
ANDERSON D M,KEAFER B A,KULIS D M,et al.An immunofluorescent survey of the brown tide chrysophyte Aureococcus anophagefferens along the northeast coast of the United States[J].Journal of Plankton Research,1993,15(5):563-580.
[82]
CARON D A,DENNETT M R,MORAN D M.Development and application of a monoclonal-antibody technique for counting Aureococcus anophagefferens,an alga causing recurrent brown tides in the Mid-Atlantic United States[J].Applied and Environmental Microbiology,2003,69(9):5492-5502.
[83]
POPELS L C,CARY S C,HUTCHINS D A,et al.The use of quantitative polymerase chain reaction for the detection and enumeration of the harmful alga Aureococcus anophagefferens in environmental samples along the United States East Coast[J].Limnology and Oceanography:Methods,2003,1(1):92-102.
[84]
SENGCO M R,LI A,TUGEND K,et al.Removal of red- and brown-tide cells using clay flocculation.I.Laboratory culture experiments with Gymnodinium breve and Aureococcus anophagefferens [J].Marine Ecology Progress Serues,2001,210:41-53.
[85]
RANDHAWA V,THAKKAR M,WEI L.Applicability of hydrogen peroxide in brown tide control-culture and microcosm studies[J].PLoS One,2012,7(10):e47844.
[86]
WEI L,WANG B,KANG R,et al.Aureococcus anophagefferens growth potential affected by coastal water toxicants[J].Journal of Applied Phycology,2013,25(1):145-152.