红色中缢虫赤潮衰亡过程中营养盐的循环和利用及对浮游植物种群组成的影响
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摘要
高生物量赤潮频繁地发生在香港的半封闭海湾,但这些海湾水体中的营养盐不足以支持如此高生物量的浮游植物生长.这些高生物量赤潮在衰亡期会释放大量无机营养盐到环境水体.我们假设这些来自赤潮衰亡释放的大量无机营养盐将加速其他种类浮游植物的生长,进而影响浮游植物种群组成.我们在香港的一个半封闭的海湾——牛尾海,利用由红色中缢虫(Mesodinium rubrum)引发的一次赤潮事件来检验这一假设.在赤潮发生水域,水体中细胞密度的达到5.0×10~5cells L~(-1),叶绿素a高达63.71μg L~(-1).在赤潮和非赤潮水域,水体中无机营养盐(硝酸盐:NO_3,铵盐:NH_4~+,磷酸盐:PO_4~3,硅酸盐:SiO_4~3)的浓度均较低.将营养盐添加到赤潮和非赤潮水体中,进行为期9天的营养盐加富培养实验.实验发现:赤潮水体中,无机营养盐的添加不能维持高细胞密度的红色中缢虫生长,第1天后红色中缢虫细胞密度迅速下降;非赤潮水体中,无机营养盐的添加并不能促使红色中缢虫细胞密度达到赤潮水体中的密度.这证实了营养盐并不是此次赤潮事件的形成或衰亡的主要驱动因素.红色中缢虫赤潮在第1天衰亡后,释放出了高浓度的NO_3、PO_4~3、SiO_4~3、NH_4~+和尿素.细菌丰度和异养活性明显增加,在第3天或第4天达到最高,并随红色中缢虫细胞密度的下降而降低.赤潮衰亡释放出来的营养盐刺激了诸如:角毛藻变种(Chaetoceros affinis var.)、卷曲鱼腥藻(circinalis)、伏氏海毛藻(Thalassiothrix frauenfeldii)和菱形藻属(Nitzschia sp.)等硅藻生长,这种刺激作用在添加SiO_4~3的处理组中更明显;同时也刺激其他藻种的生长.这些结果表明,海湾中的红色中缢虫赤潮不是直接由营养盐驱动引发的.然而,赤潮衰亡时释放的大量无机营养盐会引起寡营养环境水体中藻华的二次爆发,进而影响浮游植物种群的组成.
引文
Adams H E,Crump B C,Kling G W.2010.Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams.Environ Microbiol,12:1319-1333
Anderson D M,Glibert P M,Burkholder J M.2002.Harmful algal blooms and eutrophication:Nutrient sources,composition,and consequences.Estuaries,25:704-726
Bratbak G,Wilson W H,Heldal M.1996.Viral control of Emiliania huxleyi blooms?J Mar Syst,9:75-81
Buchan A,LeCleir G R,Gulvik C A,González J M.2014.Master recyclers:Features and functions of bacteria associated with phytoplankton blooms.Nat Rev Microbiol,12:686-698
Chrzanowski T,Kyle M.1996.Ratios of carbon,nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration.Aquat Microb Ecol,10:115-122
Crawford D W,Purdie D A,Lockwood A P M,Weissman P.1997.Recurrent red-tides in the southampton water estuary caused by the phototrophic ciliate Mesodinium rubrum.Estuar Coast Shelf Sci,45:799-812
Dagenais-Bellefeuille S,Morse D.2013.Putting the N in dinoflagellates.Front Microbiol,4:369
Dierssen H,McManus G B,Chlus A,Qiu D,Gao B C,Lin S.2015.Space station image captures a red tide ciliate bloom at high spectral and spatial resolution.Proc Natl Acad Sci USA,112:14783-14787
Donald D B,Bogard M J,Finlay K,Bunting L,Leavitt P R.2013.Phytoplankton-specific response to enrichment of phosphorus-rich surface waters with ammonium,nitrate,and urea.Plos One,8:e53277-14
Donald D B,Bogard M J,Finlay K,Leavitt P R.2011.Comparative effects of urea,ammonium,and nitrate on phytoplankton abundance,community composition,and toxicity in hypereutrophic freshwaters.Limnol Oceanogr,56:2161-2175
Dugdale R C,Wilkerson F P,Hogue V E,Marchi A.2007.The role of ammonium and nitrate in spring bloom development in San Francisco Bay.Estuar Coast Shelf Sci,73:17-29
EPD.2017.Marine Water Quality in Hong Kong in 2016.Monitoring Group,Water Policy and Planning Group,EPD,HKSAR
Fenchel T,Hansen P J.2006.Motile behaviour of the bloom-forming ciliate Mesodinium rubrum.Mar Biol Res,2:33-40
Flynn K J,Stoecker D K,Mitra A,Raven J A,Glibert P M,Hansen P J,Granéli E,Burkholder J M.2013.Misuse of the phytoplanktonzooplankton dichotomy:The need to assign organisms as mixotrophs within plankton functional types.J Plankton Res,35:3-11
Fuhrman J A,Azam F.1982.Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters:Evaluation and field results.Mar Biol,66:109-120
Fukuda R,Ogawa H,Nagata T,Koike I.1998.Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments.Appl Environ Microbiol,64:3352-3358
Glibert P M.1997.Interactions of top-down and bottom-up control in planktonic nitrogen cycling.Hydrobiologia,363:1-12
Glibert P,Seitzinger S,Heil C,Burkholder J A,Parrow M,Codispoti L,Kelly V.2005.The role of eutrophication in the global proliferation of harmful algal blooms.Oceanography,18:198-209
Glibert P M,Wilkerson F P,Dugdale R C,Parker A E,Alexander J,Blaser S,Murasko S.2014.Phytoplankton communities from San Francisco Bay Delta respond differently to oxidized and reduced nitrogen substrates-Even under conditions that would otherwise suggest nitrogen sufficiency.Front Mar Sci,1:1-16
Glibert P M,Wilkerson F P,Dugdale R C,Raven J A,Dupont C L,Leavitt P R,Parker A E,Burkholder J A M,Kana T M.2016.Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition,with emphasis on nitrogen-enriched conditions.Limnol Oceanogr,61:165-197
Gustafson D E,Stoecker D K,Johnson M D,Van Heukelem W F,Sneider K.2000.Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum.Nature,405:1049-1052
Herfort L,Peterson T D,Prahl F G,McCue L A,Needoba J A,Crump B C,Roegner G C,Campbell V,Zuber P.2012.Red waters of Myrionecta rubra are biogeochemical hotspots for the columbia river estuary with impacts on primary/secondary productions and nutrient cycles.Estuar Coast,35:878-891
Huang C,Qi Y.1997.The abundance cycle and influence factors on red tide phenomena of Noctiluca scintillans(Dinophyceae)in Dapeng Bay,the South China Sea.J Plankton Res,19:303-318
Jiang H,Johnson M D.2017.Jumping and overcoming diffusion limitation of nutrient uptake in the photosynthetic ciliate Mesodinium rubrum.Limnol Oceanogr,62:421-436
Knap A H,Michaels A,Close A R,Ducklow H,Dickson A G.1996.Protocols for the joint global ocean flux study(JGOFS)core measurements.JGOFS,Reprint of the IOC Manuals and Guides No.29,UNESCO 1994,19
Lai Z,Yin K.2014.Physical-biological coupling induced aggregation mechanism for the formation of high biomass red tides in low nutrient waters.Harmful Algae,31:66-75
Liu H,Song X,Huang L,Tan Y,Zhang J.2011.Phytoplankton biomass and production in northern South China Sea during summer:Influenced by Pearl River discharge and coastal upwelling.Acta Ecologica Sin,31:133-136
Lomas M W,Glibert P M.1999.Temperature regulation of nitrate uptake:A novel hypothesis about nitrate uptake and reduction in cool-water diatoms.Limnol Oceanogr,44:556-572
Lomas M W,Rumbley C J,Glibert P M.2000.Ammonium release by nitrogen sufficient diatoms in response to rapid increases in irradiance.J Plankton Res,22:2351-2366
Mccarthy J J,Goldman J C.1979.Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters.Science,203:670-672
Mitra A,Flynn K J.2010.Modelling mixotrophy in harmful algal blooms:More or less the sum of the parts?J Mar Syst,83:158-169
Myung G,Kim H S,Park J W,Park J S,Yih W.2013.Sequestered plastids in Mesodinium rubrum are functionally active up to 80 days of phototrophic growth without cryptomonad prey.Harmful Algae,27:82-87
Parker A E,Hogue V E,Wilkerson F P,Dugdale R C.2012.The effect of inorganic nitrogen speciation on primary production in the San Francisco Estuary.Estuar Coast Shelf Sci,104-105:91-101
Porter K G,Feig Y S.1980.The use of DAPI for identifying and counting aquatic microflora1.Limnol Oceanogr,25:943-948
Price N M,Harrison P J.1987.Comparison of methods for the analysis of dissolved urea in seawater.Mar Biol,94:307-317
Raven J A.1991.Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton:Relation to increased CO2and temperature.Plant Cell Environ,14:779-794
Raven J A.2011.The cost of photoinhibition.Physiologia Plantarum,142:87-104
Saba G K,Steinberg D K,Bronk D A,Place A R.2011.The effects of harmful algal species and food concentration on zooplankton grazer production of dissolved organic matter and inorganic nutrients.Harmful Algae,10:291-303
Shiah F K,Ducklow H W.1994.Temperature and substrate regulation of bacterial abundance,production and specific growth rate in Chesapeake Bay,USA.Mar Ecol Prog Ser,103:297-308
Sinsabaugh R L,Shah J J F.2010.Integrating resource utilization and temperature in metabolic scaling of riverine bacterial production.Ecology,91:1455-1465
Slawyk G,Macisaac J J.1972.Comparison of two automated ammonium methods in a region of coastal upwelling.Deep Sea Res Oceanogr Abstr,19:521-524
Tong M,Smith J L,Kulis D M,Anderson D M.2015.Role of dissolved nitrate and phosphate in isolates of Mesodinium rubrum and toxinproducing Dinophysis acuminata.Aquat Microb Ecol,75:169-185
Vrede K,Heldal M,Norland S,Bratbak G.2002.Elemental composition(C,N,P)and cell volume of exponentially growing and nutrient-limited bacterioplankton.Appl Environ Microbiol,68:2965-2971
Wilkerson F P,Dugdale R C,Hogue V E,Marchi A.2006.Phytoplankton blooms and nitrogen productivity in San Francisco Bay.Estuar Coast,29:401-416
Yih W,Kim H S,Jeong H J,Myung G,Kim Y G.2004.Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum.Aquat Microb Ecol,36:165-170
Yih W,Kim H S,Myung G,Park J W,Yoo Y D,Jeong H J.2013.The red-tide ciliate Mesodinium rubrum in Korean coastal waters.Harmful Algae,30:S53-S61
Yin K.2003.Influence of monsoons and oceanographic processes on red tides in Hong Kong waters.Mar Ecol Prog Ser,262:27-41
Yin K,Song X X,Liu S,Kan J,Qian P Y.2008.Is inorganic nutrient enrichment a driving force for the formation of red tides?Harmful Algae,8:54-59
Anderson D M,Glibert P M,Burkholder J M.2002.Harmful algal blooms and eutrophication:Nutrient sources,composition,and consequences.Estuaries,25:704-726
Bratbak G,Wilson W H,Heldal M.1996.Viral control of Emiliania huxleyi blooms?J Mar Syst,9:75-81
Buchan A,LeCleir G R,Gulvik C A,González J M.2014.Master recyclers:Features and functions of bacteria associated with phytoplankton blooms.Nat Rev Microbiol,12:686-698
Chrzanowski T,Kyle M.1996.Ratios of carbon,nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration.Aquat Microb Ecol,10:115-122
Crawford D W,Purdie D A,Lockwood A P M,Weissman P.1997.Recurrent red-tides in the southampton water estuary caused by the phototrophic ciliate Mesodinium rubrum.Estuar Coast Shelf Sci,45:799-812
Dagenais-Bellefeuille S,Morse D.2013.Putting the N in dinoflagellates.Front Microbiol,4:369
Dierssen H,McManus G B,Chlus A,Qiu D,Gao B C,Lin S.2015.Space station image captures a red tide ciliate bloom at high spectral and spatial resolution.Proc Natl Acad Sci USA,112:14783-14787
Donald D B,Bogard M J,Finlay K,Bunting L,Leavitt P R.2013.Phytoplankton-specific response to enrichment of phosphorus-rich surface waters with ammonium,nitrate,and urea.Plos One,8:e53277-14
Donald D B,Bogard M J,Finlay K,Leavitt P R.2011.Comparative effects of urea,ammonium,and nitrate on phytoplankton abundance,community composition,and toxicity in hypereutrophic freshwaters.Limnol Oceanogr,56:2161-2175
Dugdale R C,Wilkerson F P,Hogue V E,Marchi A.2007.The role of ammonium and nitrate in spring bloom development in San Francisco Bay.Estuar Coast Shelf Sci,73:17-29
EPD.2017.Marine Water Quality in Hong Kong in 2016.Monitoring Group,Water Policy and Planning Group,EPD,HKSAR
Fenchel T,Hansen P J.2006.Motile behaviour of the bloom-forming ciliate Mesodinium rubrum.Mar Biol Res,2:33-40
Flynn K J,Stoecker D K,Mitra A,Raven J A,Glibert P M,Hansen P J,Granéli E,Burkholder J M.2013.Misuse of the phytoplanktonzooplankton dichotomy:The need to assign organisms as mixotrophs within plankton functional types.J Plankton Res,35:3-11
Fuhrman J A,Azam F.1982.Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters:Evaluation and field results.Mar Biol,66:109-120
Fukuda R,Ogawa H,Nagata T,Koike I.1998.Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments.Appl Environ Microbiol,64:3352-3358
Glibert P M.1997.Interactions of top-down and bottom-up control in planktonic nitrogen cycling.Hydrobiologia,363:1-12
Glibert P,Seitzinger S,Heil C,Burkholder J A,Parrow M,Codispoti L,Kelly V.2005.The role of eutrophication in the global proliferation of harmful algal blooms.Oceanography,18:198-209
Glibert P M,Wilkerson F P,Dugdale R C,Parker A E,Alexander J,Blaser S,Murasko S.2014.Phytoplankton communities from San Francisco Bay Delta respond differently to oxidized and reduced nitrogen substrates-Even under conditions that would otherwise suggest nitrogen sufficiency.Front Mar Sci,1:1-16
Glibert P M,Wilkerson F P,Dugdale R C,Raven J A,Dupont C L,Leavitt P R,Parker A E,Burkholder J A M,Kana T M.2016.Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition,with emphasis on nitrogen-enriched conditions.Limnol Oceanogr,61:165-197
Gustafson D E,Stoecker D K,Johnson M D,Van Heukelem W F,Sneider K.2000.Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum.Nature,405:1049-1052
Herfort L,Peterson T D,Prahl F G,McCue L A,Needoba J A,Crump B C,Roegner G C,Campbell V,Zuber P.2012.Red waters of Myrionecta rubra are biogeochemical hotspots for the columbia river estuary with impacts on primary/secondary productions and nutrient cycles.Estuar Coast,35:878-891
Huang C,Qi Y.1997.The abundance cycle and influence factors on red tide phenomena of Noctiluca scintillans(Dinophyceae)in Dapeng Bay,the South China Sea.J Plankton Res,19:303-318
Jiang H,Johnson M D.2017.Jumping and overcoming diffusion limitation of nutrient uptake in the photosynthetic ciliate Mesodinium rubrum.Limnol Oceanogr,62:421-436
Knap A H,Michaels A,Close A R,Ducklow H,Dickson A G.1996.Protocols for the joint global ocean flux study(JGOFS)core measurements.JGOFS,Reprint of the IOC Manuals and Guides No.29,UNESCO 1994,19
Lai Z,Yin K.2014.Physical-biological coupling induced aggregation mechanism for the formation of high biomass red tides in low nutrient waters.Harmful Algae,31:66-75
Liu H,Song X,Huang L,Tan Y,Zhang J.2011.Phytoplankton biomass and production in northern South China Sea during summer:Influenced by Pearl River discharge and coastal upwelling.Acta Ecologica Sin,31:133-136
Lomas M W,Glibert P M.1999.Temperature regulation of nitrate uptake:A novel hypothesis about nitrate uptake and reduction in cool-water diatoms.Limnol Oceanogr,44:556-572
Lomas M W,Rumbley C J,Glibert P M.2000.Ammonium release by nitrogen sufficient diatoms in response to rapid increases in irradiance.J Plankton Res,22:2351-2366
Mccarthy J J,Goldman J C.1979.Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters.Science,203:670-672
Mitra A,Flynn K J.2010.Modelling mixotrophy in harmful algal blooms:More or less the sum of the parts?J Mar Syst,83:158-169
Myung G,Kim H S,Park J W,Park J S,Yih W.2013.Sequestered plastids in Mesodinium rubrum are functionally active up to 80 days of phototrophic growth without cryptomonad prey.Harmful Algae,27:82-87
Parker A E,Hogue V E,Wilkerson F P,Dugdale R C.2012.The effect of inorganic nitrogen speciation on primary production in the San Francisco Estuary.Estuar Coast Shelf Sci,104-105:91-101
Porter K G,Feig Y S.1980.The use of DAPI for identifying and counting aquatic microflora1.Limnol Oceanogr,25:943-948
Price N M,Harrison P J.1987.Comparison of methods for the analysis of dissolved urea in seawater.Mar Biol,94:307-317
Raven J A.1991.Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton:Relation to increased CO2and temperature.Plant Cell Environ,14:779-794
Raven J A.2011.The cost of photoinhibition.Physiologia Plantarum,142:87-104
Saba G K,Steinberg D K,Bronk D A,Place A R.2011.The effects of harmful algal species and food concentration on zooplankton grazer production of dissolved organic matter and inorganic nutrients.Harmful Algae,10:291-303
Shiah F K,Ducklow H W.1994.Temperature and substrate regulation of bacterial abundance,production and specific growth rate in Chesapeake Bay,USA.Mar Ecol Prog Ser,103:297-308
Sinsabaugh R L,Shah J J F.2010.Integrating resource utilization and temperature in metabolic scaling of riverine bacterial production.Ecology,91:1455-1465
Slawyk G,Macisaac J J.1972.Comparison of two automated ammonium methods in a region of coastal upwelling.Deep Sea Res Oceanogr Abstr,19:521-524
Tong M,Smith J L,Kulis D M,Anderson D M.2015.Role of dissolved nitrate and phosphate in isolates of Mesodinium rubrum and toxinproducing Dinophysis acuminata.Aquat Microb Ecol,75:169-185
Vrede K,Heldal M,Norland S,Bratbak G.2002.Elemental composition(C,N,P)and cell volume of exponentially growing and nutrient-limited bacterioplankton.Appl Environ Microbiol,68:2965-2971
Wilkerson F P,Dugdale R C,Hogue V E,Marchi A.2006.Phytoplankton blooms and nitrogen productivity in San Francisco Bay.Estuar Coast,29:401-416
Yih W,Kim H S,Jeong H J,Myung G,Kim Y G.2004.Ingestion of cryptophyte cells by the marine photosynthetic ciliate Mesodinium rubrum.Aquat Microb Ecol,36:165-170
Yih W,Kim H S,Myung G,Park J W,Yoo Y D,Jeong H J.2013.The red-tide ciliate Mesodinium rubrum in Korean coastal waters.Harmful Algae,30:S53-S61
Yin K.2003.Influence of monsoons and oceanographic processes on red tides in Hong Kong waters.Mar Ecol Prog Ser,262:27-41
Yin K,Song X X,Liu S,Kan J,Qian P Y.2008.Is inorganic nutrient enrichment a driving force for the formation of red tides?Harmful Algae,8:54-59