Difference between revisions of "Harmful algal bloom"

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Socio-economic costs cannot easily be quantified, but they are considerable<ref name=Ber16/> . 
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Socio-economic costs cannot easily be quantified, but they are considerable<ref>Hoagland P. and Scatasta S. (2006) The economic effects of harmful algal blooms. In Graneli E. and Turner J.T. (eds) Ecology of harmful algae. New York, NY: Springer-Verlag, pp. 391–402</ref><ref name=Ber16/><ref>Ross Brown, A., Lilley, M., Shutler, J., Lowe, C., Artioli, Y, Torres, R., Berdalet, E. and Tyler, C.R. 2019. Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries. Rev. Aquacult. 1–26</ref>. 
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Estimates are in the order of US$100 million per year in the United States, mainly related to aquaculture losses. A much higher estimate of about US $ 1 billion per year was estimated for Europe, mainly due to losses related to (not necessarily toxic) algal blooms affecting the attractiveness of beaches for coastal tourists<ref>Hoagland P. and Scatasta S. (2006) The economic effects of harmful algal blooms. In Graneli E. and Turner J.T. (eds) Ecology of harmful algae. New York, NY: Springer-Verlag, pp. 391–402</ref>.  
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Estimates are in the order of several billon US$ annually up to about 8 billion US$, related to precautionary closure of mariculture farms, reduced attractiveness of beaches for coastal tourists and economic impacts of marine phycotoxins on human health.  
  
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The greatest direct effect of HABs concerns aquaculture. Aquaculture has experienced tremendous growth in recent decades and has become a food source on which much of the world's population depends. As the growth of aquaculture is expected to continue, harmful algal blooms are an increasing threat. The paradox is that the waste from finfish farms itself promotes conditions for the development of HABs<ref>Anderson, D. 2012. HABs in a changing world: a perspective on harmful algal blooms, their impacts, and research and management in a dynamic era of climactic and environmental change. Harmful Algae 2012 (2012). 2014 ; 2012: 3–17 PMID: 26640829; PMCID: PMC4667985</ref><ref> Strain, P. M., and Hargrave, B. T. 2005. Salmon aquaculture, nutrient fluxes and ecosystem processes in Southwestern New Brunswick, in Environmental Effects of Marine Finfish Aquaculture, Handbook of Environmental Chemistry, ed. B. T. Hargrave (Berlin: Springer): 29–57</ref>.
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The greatest direct effect of HABs concerns mariculture. Mariculture has experienced tremendous growth in recent decades and has become a food source on which much of the world's population depends. As the growth of mariculture is expected to continue, harmful algal blooms are an increasing threat. The paradox is that the waste from finfish farms itself promotes conditions for the development of HABs<ref>Anderson, D. 2012. HABs in a changing world: a perspective on harmful algal blooms, their impacts, and research and management in a dynamic era of climactic and environmental change. Harmful Algae 2012 (2012). 2014 ; 2012: 3–17 PMID: 26640829; PMCID: PMC4667985</ref><ref> Strain, P. M., and Hargrave, B. T. 2005. Salmon aquaculture, nutrient fluxes and ecosystem processes in Southwestern New Brunswick, in Environmental Effects of Marine Finfish Aquaculture, Handbook of Environmental Chemistry, ed. B. T. Hargrave (Berlin: Springer): 29–57</ref>.
  
  
 
==Conditions favouring the development of harmful algal blooms==
 
==Conditions favouring the development of harmful algal blooms==
  
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HABs are natural phenomena, but these events can be favoured by anthropogenic pressures in coastal areas. It is not known exactly how toxin producing algae develop. What is known, however, is that most toxic algae belong to the class of flagellates and cyanobacteria. Environmental conditions favorable for the development of flagellates and cyanobacteria therefore create the greatest risk for the development of HABs. Among the algae of the diatom class there are also toxic species, but these are rarer than among the flagellates. The following is known about the shift from conditions favorable for the development of diatoms to conditions favorable for the development of flagellates and cyanobacteria:
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HABs are natural phenomena, but these events can be favoured by anthropogenic pressures in coastal areas. It is not known exactly how toxin producing algae develop. What is known, however, is that most toxic algae belong to the class of flagellates and cyanobacteria. Environmental conditions favorable for the development of flagellates and cyanobacteria therefore create the greatest risk for the development of HABs. Among the algae of the diatom class (large plankton with silica cell wall) there are also toxic species, but these are rarer than among the flagellates. The following is known about the shift from conditions favorable for the development of diatoms to conditions favorable for the development of flagellates and cyanobacteria, thus promoting the occurrence of harmful algal blooms:
  
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# Higher temperatures. The optimal growth of diatoms occurs at relatively low temperatures compared to flagellates and cyanobacteria<ref>Anderson, N.J. 2000. Diatoms, temperature and climate change. Eur. J. Phycol. 35: 307–314</ref>. Experiments show that the occurrence of HABs increases with temperature<ref>Paerl, H.W. and Scott, J.T. 2010. Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environ. Sci. Technol. 44: 7756–7758</ref>. Warmer waters are thought to favor smaller-sized cells as they are more efficient in harvesting light and nutrients and maintaining their position in the euphotic zone<ref>Daufresne, M., Lengefellner, K. and Sommer, U. 2009. Global warming benefits the small in
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# Higher temperatures. The optimal growth of diatoms occurs at relatively low temperatures compared to flagellates and cyanobacteria<ref>Anderson, N.J. 2000. Diatoms, temperature and climate change. Eur. J. Phycol. 35: 307–314</ref>. This is consistent with experiments that show increasing occurrence of HABs with temperature<ref>Paerl, H.W. and Scott, J.T. 2010. Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environ. Sci. Technol. 44: 7756–7758</ref>. Warmer waters are thought to also favour smaller-sized cells (less diatoms and more potentially harmful flagellates and cyanobacteria) as they are more efficient in harvesting light and nutrients and maintaining their position in the euphotic zone<ref>Daufresne, M., Lengefellner, K. and Sommer, U. 2009. Global warming benefits the small in aquatic ecosystems. Proc. Natl. Acad. Sci. U. S. A. 106: 12788–12793<ref>. Cyanobacteria dominate in warm nutrient-poor water <ref>Maranon, E., Cermeno, P., Latasa, M. and Tadonleke, R.D. 2012. Temperature, resources, and phytoplankton size structure in the ocean. Limnol. Oceanogr. 67: 1266–1278</ref>.  
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aquatic ecosystems. Proc. Natl. Acad. Sci. U. S. A. 106: 12788–12793<ref>. Cyanobacteria dominate in warm nutrient-poor water <ref>Maranon, E., Cermeno, P., Latasa, M. and Tadonleke, R.D. 2012. Temperature, resources, and phytoplankton size structure in the ocean. Limnol. Oceanogr. 67: 1266–1278</ref>.  
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# A high ratio of dissolved nitrogen N versus phosphorus P. This has several causes: (a) Very small cells, such as picocyanobacteria, have a lower requirement for P due to the smaller need for structural components in the cell<ref>Finkel, Z.V., J. Beardall, K.J. Flynn, A. Quiqq, T.A.V. Rees, and J.A. Raven. 2010. Phytoplankton in a changing world: Cell size and elemental stoichiometry. Journal of Plankton Research 32:119–137</ref>; (b) Many harmful dinoflagellates are mixotrophic <ref>Mitra, A. and Flynn, K.J. 2010. Modelling mixotrophy in harmful algal blooms: more or less the sum of the parts? J. Mar. Syst. 83: 58–169</ref><ref>Stoecker, D., Tillmann, U. and Graneli, E. 2006. Phagotrophy in harmful algae. In: Graneli, E. and Turner, J. (eds) Ecology of Harmful Algae, Series: Ecological Studies, Vol. 189, Springer Verlag, Heidelberg, pp 177–187</ref>, which means that they can ingest dissolved and particulate organic material and thus correct an imbalance in the  [[Stoichiometry|stoichiometric]] N:P ratio<ref>Burkholder, J.M., Glibert, P.M. and Skelton, H. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8: 77–93</ref><ref>Jeong, H.J., Yoo, Y.D., Kim, J.S., Seong, K.A., Kang, N.S. and Kim, T.H., 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45: 65–91</ref><ref>Flynn, K.J., Stoecker, D.K., Mitra, A., Raven, J.A., Glibert, P.M., Hansen, P.J., Graneli, E. and Burkholder, J.M. 2013. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J. Plankt. Res 35: 3–11</ref>; (c) Harmful algae can release excess N via toxins <ref name=G16>Glibert, P.M., Wilkerson, F.P., Dugdale, R.C., Raven, J.A., Dupont, C., Leavitt, P.R., Parker, A.E., Burkholder, J.M. and 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</ref>. Many cyanobacteria and marine dinoflagellate HABs are more toxic when N is in stoichiometric excess over P. In the dinoflagellate ''Alexandrium tamarense'', saxitoxin production has been shown to increase by three- to fourfold under P deficiency<ref>Graneli, E., and Flynn, K.J. 2006. Chemical and physical factors influencing toxin content. Pp. 229–241 in Ecology of Harmful Algae. E. Graneli, and J.T. Turner, eds, Springer, Heidelberg, Germany</ref>. Increasing N:P ratios in ecosystems therefore shift communities toward systems with trait dominance of higher optimal N:P ratios (higher P uptake affinity and decreasing N retention) which is a typical HAB trait<ref>Meunier, C.L., Boersma, M., El-Sabaawi, R., Halvorson, H.M., Herstoff, E.M., Van de Waal, D.B., Vogt, R.J. and Litchman, E. 2017. From elements to function: toward unifying ecological stoichiometry and trait-based ecology. Front. Environ. Sci 5, 18</ref>.
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# A high ratio of dissolved nitrogen N versus phosphorus P. This has several causes: (a) Very small cells, such as picocyanobacteria, have a lower requirement for P due to the smaller need for structural components in the cell<ref>Finkel, Z.V., J. Beardall, K.J. Flynn, A. Quiqq, T.A.V. Rees, and J.A. Raven. 2010. Phytoplankton in a changing world: Cell size and elemental stoichiometry. Journal of Plankton Research 32:119–137</ref>; (b) Many dinoflagellates are mixotrophic <ref>Mitra, A. and Flynn, K.J. 2010. Modelling mixotrophy in harmful algal blooms: more or less the sum of the parts? J. Mar. Syst. 83: 58–169</ref><ref>Stoecker, D., Tillmann, U. and Graneli, E. 2006. Phagotrophy in harmful algae. In: Graneli, E. and Turner, J. (eds) Ecology of Harmful Algae, Series: Ecological Studies, Vol. 189, Springer Verlag, Heidelberg, pp 177–187</ref>, which means that they can ingest dissolved and particulate organic material and thus correct an imbalance in the  [[Stoichiometry|stoichiometric]] N:P ratio<ref>Burkholder, J.M., Glibert, P.M. and Skelton, H. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8: 77–93</ref><ref>Jeong, H.J., Yoo, Y.D., Kim, J.S., Seong, K.A., Kang, N.S. and Kim, T.H., 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45: 65–91</ref><ref>Flynn, K.J., Stoecker, D.K., Mitra, A., Raven, J.A., Glibert, P.M., Hansen, P.J., Graneli, E. and Burkholder, J.M. 2013. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J. Plankt. Res 35: 3–11</ref>; (c) Harmful algae can release excess N via toxins <ref name=G16>Glibert, P.M., Wilkerson, F.P., Dugdale, R.C., Raven, J.A., Dupont, C., Leavitt, P.R., Parker, A.E., Burkholder, J.M. and 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</ref>. Many cyanobacteria and marine dinoflagellate HABs are more toxic when N is in stoichiometric excess over P. In the dinoflagellate ''Alexandrium tamarense'', saxitoxin production has been shown to increase by three- to fourfold under P deficiency<ref>Graneli, E., and Flynn, K.J. 2006. Chemical and physical factors influencing toxin content. Pp. 229–241 in Ecology of Harmful Algae. E. Graneli, and J.T. Turner, eds, Springer, Heidelberg, Germany</ref>.  
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# Increasing proportions of N in the form of ammonium and urea (CO(NH<sub>2</sub>)<sub>2</sub>). Causes: (a) Potentially harmful flagellates and cyanobacteria grow better on ammonium (NH<sub>4</sub><sup>+</sup>) whereas diatoms prefer nitrate (NO<sub>3</sub><sup>-</sup>)<ref name=G17>Glibert, P.M. 2017. Eutrophication, harmful algae and biodiversity - challenging paradigms in a world of complex nutrient changes. Mar. Poll. Bull. 124: 591–606</ref>; (b) Mixotrophic harmful dinoflagellates can use urea as food source<ref name=G14>Glibert, P.M., Manager, R., Sobota, D.J., Bouwman, L. 2014. The Haber-Bosch-Harmful algal bloom (HB-HAB) link. Environ. Res. Lett. 9, 105001</ref>.
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# Increasing proportions of N in the form of ammonium and urea (CO(NH<sub>2</sub>)<sub>2</sub>). Causes: (a) Diatoms grow better on nitrate (NO<sub>3</sub><sup>-</sup>) whereas flagellates and cyanobacteria prefer ammonium (NH<sub>4</sub><sup>+</sup>) <ref name=G17>Glibert, P.M. 2017. Eutrophication, harmful algae and biodiversity - challenging paradigms in a world of complex nutrient changes. Mar. Poll. Bull. 124: 591–606</ref>; (b) Mixotrophic dinoflagellates can use urea as food source<ref name=G14>Glibert, P.M., Manager, R., Sobota, D.J., Bouwman, L. 2014. The Haber-Bosch-Harmful algal bloom (HB-HAB) link. Environ. Res. Lett. 9, 105001</ref>.
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# Enhancement of stratified conditions<ref>Telesh, I., Schubert, H. and Skarlato, S. 2021. Abiotic stability promotes dinoflagellate blooms in marine coastal ecosystems. Estuarine, Coastal and Shelf Science 251, 107239</ref>. Causes for favouring potentially harmful flagellates and cyanobacteria over diatoms are: (a) Larger phytoplankton sinks more easily out of the photic zone, thus smaller plankton dominates <ref>Winder, M., Reuter, J.E. and Schladow, S.G. 2009. Lake warming favours small-sized plankton diatom species. Proc. Roy. Soc B 276: 427–435</ref>; (b) Many harmful dinoflagellates are mixotrophs which can swim to the pycnocline to capture organic prey<ref>Stoecker, D.K., Hansen, P.J., Caron, D.A. and Mitra, A. 2017. Mixotrophy in the marine plankton. Ann. Rev. Mar. Sci. 9: 311–335</ref>.  
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# Enhancement of stratified conditions. Causes are: (a) Larger phytoplankton sinks more easily out of the photic zone, thus smaller plankton dominates <ref>Winder, M., Reuter, J.E. and Schladow, S.G. 2009. Lake warming favours small-sized plankton diatom species. Proc. Roy. Soc B 276: 427–435</ref>; (b) Many harmful dinoflagellates are mixotrophs which can swim to the pycnocline to capture organic prey<ref>Stoecker, D.K., Hansen, P.J., Caron, D.A. and Mitra, A. 2017. Mixotrophy in the marine plankton. Ann. Rev. Mar. Sci. 9: 311–335</ref>.  
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# Reduction of the Si:N ratio. Diatoms require Si for growth; Si limitation favours non-Si species such as flagellates and cyanobacteria<ref name=M14>Maavara, T., Dürr, H.H. and Van Cappellen, P. 2014. Worldwide retention of nutrient silicon by river damming: from sparse data set to global estimate. Glob. Biogeochem. Cycl. 28: 842–855</ref>.
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# Retention of Si in reservoirs behind river dams. Diatoms require Si for growth; Si limitation favours non-Si species such as flagellates and cyanobacteria<ref>Maavara, T., Dürr, H.H. and Van Cappellen, P. 2014. Worldwide retention of nutrient silicon by river damming: from sparse data set to global estimate. Glob. Biogeochem. Cycl. 28: 842–855</ref><ref>Maavara, T., Parsons, C.T., Ridenour, C., Stojanovic, S., Dürr, H.H., Powley, H.R. and Van Cappellen, P. 2015. Global phosphorus retention by river damming. Proc. Natl. Acad. Sci. U. S. A. 112, 15603–15608</ref>.
 
  
  
 
==Causes for an increase in HABs==
 
==Causes for an increase in HABs==
  
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Although no quantitative estimates can be given, there is strong evidence that the occurrence of harmful algal blooms has increased during the past decades. The causes for an increase in HABs are related to the furtherance of the above mentioned conditions favorable to their development. Probable causes are:
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Although no quantitative estimates can be given, there is strong evidence that the occurrence of harmful algal blooms has increased during the past decades. The causes for an increase in HABs are related to the furtherance of the above mentioned conditions favorable to their development. Probable causes are<ref>Glibert, P.M. 2020. Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae 91, 101583</ref>:
  
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# Increase of nitrogen-rich effluents and atmospheric emissions to the sea. The main cause is the increasing use of fertilizers; in the period 1970-2000 the N-fertilizer use has increased much faster than the P-fertilizer use (see Fig. 1)<ref name=GB>Glibert, P.M. and Burford, M.A. 2017. Globally changing nutrient loads and harmful algal blooms: Recent advances, new paradigms, and continuing challenges. Oceanography 30: 58–69</ref>. Only about half of the fertilizer N is taken up by crops; the remainder is partly stored in the soil and partly emitted to the sea via runoff and the atmosphere. Other N-rich sources are the widespread and expanding fish farms, which release N mainly in chemically reduced form (e.g., ammonium, dissolved organic N, DON)<ref>Bouwman, A.F., Beusen, A.H.W., Glibert, P.M., Overbeck, C., Pawlowski, M., Silveiva, J.H., Mulsow, S., Yu, R. and Zhou, M.J. 2013. Mariculture: significant and expanding cause of coastal nutrient enrichment. Environ. Res. Lett. 8, 044026</ref>.  
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# Increase of nitrogen-rich effluents and atmospheric emissions to the sea. It has been estimated that the atmospheric deposition of nutrients in the ocean is now about 20-fold greater than the Redfield ratio for N:P. The main cause is the increasing use of fertilizers; in the period 1970-2000 the N-fertilizer use has increased much faster than the P-fertilizer use (see Fig. 1) <ref name=P>Penuelas, J., Poulter, B., Sardans, J., Ciais, P., van der Velde, M., Bopp, L., et al. 2013. Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4: 2934</ref>. Only about half of the fertilizer N is taken up by crops; the remainder is partly stored in the soil and partly emitted to the sea via runoff and the atmosphere. Other N-rich sources are the widespread and expanding fish farms, which release N mainly in chemically reduced form (e.g., ammonium, dissolved organic N, DON)<ref>Bouwman, A.F., Beusen, A.H.W., Glibert, P.M., Overbeck, C., Pawlowski, M., Silveiva, J.H., Mulsow, S., Yu, R. and Zhou, M.J. 2013. Mariculture: significant and expanding cause of coastal nutrient enrichment. Environ. Res. Lett. 8, 044026</ref>. The increase of the N:P ratio is further due to the more efficient reduction of P compared to N in sewage treatment plants and the reduction of P in laundry products.  
 
# Fertilizer effluents and emissions produce a shift from nitrate to ammonium and urea, which favours HABs<ref name=G16/><ref name=G14/>.
 
# Fertilizer effluents and emissions produce a shift from nitrate to ammonium and urea, which favours HABs<ref name=G16/><ref name=G14/>.
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# Effect of river dams. Large fractions of the fluvial P load (about 43% of total dissolved P and reactive particulate P) and Si load (about 20% of dissolved Si and reactive particulate Si) are bound to sediments that are retained in upstream reservoirs, whereas about 90% of the total N load is unaffected<ref name=M14/><ref>Maavara, T., Parsons, C.T., Ridenour, C., Stojanovic, S., Dürr, H.H., Powley, H.R. and Van Cappellen, P. 2015. Global phosphorus retention by river damming. Proc. Natl. Acad. Sci. U. S. A. 112, 15603–15608</ref>. This result in an increase in the N:P and N:Si ratios of riverine delivery to coastal areas following dam construction.
 
# Effects of climate change: (a) Rising seawater temperatures; (b) Intensification of sea water stratification; (c) Increase in peak river discharges and corresponding increase in nitrogen supply in coastal waters<ref>Howarth, R.W., Swaney, D.P., Boyer, E.W., Marino, R., Jaworski, N. and Goodale, C. 2006. The influence of climate on average nitrogen export from large watersheds in the Northeastern United States. Biogeochemistry 79: 163–186</ref>; (d) Increase in nutrient concentrations associated with intensification of upwelling events<ref>Goes, J.I., Thoppil, P.G., Gomes, H.D.R. and Fasullo, J.T. 2005. Warming of the Eurasian landmass is making the Arabian Sea more productive. Science 308: 545–547</ref>.
 
# Effects of climate change: (a) Rising seawater temperatures; (b) Intensification of sea water stratification; (c) Increase in peak river discharges and corresponding increase in nitrogen supply in coastal waters<ref>Howarth, R.W., Swaney, D.P., Boyer, E.W., Marino, R., Jaworski, N. and Goodale, C. 2006. The influence of climate on average nitrogen export from large watersheds in the Northeastern United States. Biogeochemistry 79: 163–186</ref>; (d) Increase in nutrient concentrations associated with intensification of upwelling events<ref>Goes, J.I., Thoppil, P.G., Gomes, H.D.R. and Fasullo, J.T. 2005. Warming of the Eurasian landmass is making the Arabian Sea more productive. Science 308: 545–547</ref>.
 
# Spreading of harmful algae species across the oceans by increased transport of algae with ship ballast water<ref name=Ber16/>.
 
# Spreading of harmful algae species across the oceans by increased transport of algae with ship ballast water<ref name=Ber16/>.
  
  
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[[File:FertilizerUseNP.jpg|thumb|600px|center|Fig. 1. N and P content of global fertilizer use. After Glibert and Burford (2017<ref name=GB/>) and FAO (2019<ref name=FAO>FAO. 2019. World fertilizer trends and outlook to 2022. FAO, Rome</ref>).]]
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[[File:FertilizerUseNP.jpg|thumb|600px|center|Fig. 1. N and P content of global fertilizer use. After Glibert and Burford (2017<ref name=GB>Glibert, P.M. and Burford, M.A. 2017. Globally changing nutrient loads and harmful algal blooms: Recent advances, new paradigms, and continuing challenges. Oceanography 30: 58–69</ref>) and FAO (2019<ref name=FAO>FAO. 2019. World fertilizer trends and outlook to 2022. FAO, Rome</ref>).]]
  
  
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The factors that promote the occurrence of HABs are expected to become more important in the future. This holds in the first place for global warming and for eutrophication, in particular the nitrogen component of eutrophication. Efforts to combat harmful algal blooms are vital, but simple solutions do not exist. It is widely recognized that action is needed to halt global climate change and to reduce nitrogen emissions from agriculture. To this end, agreements have been made and initiatives have been developed at various administrative levels. Important international frameworks have been set up for climate policy that will eventually reverse the trend of global warming. A comparable encompassing agreement has not yet been established for agricultural emissions, although in Europe the [[Nitrates Directive]] has been in force since 1991. This directive has contributed to a reduction in N emissions from European agriculture<ref>Velthof G.L., Lesschen, J.P., Webb, J., Pietrzak, S., Miatkowski, Z., Pinto, M., Kros, J. and Oenema, O. 2014.The impact of the Nitrates Directive on nitrogen emissions from agriculture in the EU-27during 2000–2008. Science of the Total Environment 468–469: 1225–1233</ref> - however, without special focus on the nitrate: ammonium ratio of the emissions.  
 
The factors that promote the occurrence of HABs are expected to become more important in the future. This holds in the first place for global warming and for eutrophication, in particular the nitrogen component of eutrophication. Efforts to combat harmful algal blooms are vital, but simple solutions do not exist. It is widely recognized that action is needed to halt global climate change and to reduce nitrogen emissions from agriculture. To this end, agreements have been made and initiatives have been developed at various administrative levels. Important international frameworks have been set up for climate policy that will eventually reverse the trend of global warming. A comparable encompassing agreement has not yet been established for agricultural emissions, although in Europe the [[Nitrates Directive]] has been in force since 1991. This directive has contributed to a reduction in N emissions from European agriculture<ref>Velthof G.L., Lesschen, J.P., Webb, J., Pietrzak, S., Miatkowski, Z., Pinto, M., Kros, J. and Oenema, O. 2014.The impact of the Nitrates Directive on nitrogen emissions from agriculture in the EU-27during 2000–2008. Science of the Total Environment 468–469: 1225–1233</ref> - however, without special focus on the nitrate: ammonium ratio of the emissions.  
  
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Local reduction of nutrient concentrations can be achieved by harvesting marine products that grow on nutrients and provide economic value (benefit from ecosystem goods and services) <ref>Burkholder, J. M., and Shumway, S.E. 2011. Bivalve shellfish aquaculture and eutrophication, in Shellfish Aquaculture and the Environment, ed. S.E. Shumway (Hoboken, NY: John Wiley & Sons, Inc.), 155–215</ref><ref>Petersen, J.K., Holmer, M., Termansen, M., Hasler, B. 2019. Nutrient extraction through bivalves. In: Smaal, A.C., Ferreira, J.G., Grant, J., Petersen, J.K., Strand, O. (Eds.), Goods and Services of Marine Bivalves. Springer, Cham, pp. 179–208</ref>. Examples are the harvesting of farmed mussels<ref>Kotta, J., Futter, M., Kaasik, A., Liversage, K., Rätsep, M., Barboza, F. R., et al. 2020. Cleaning up seas using blue growth initiatives: mussel farming for eutrophication control in the Baltic Sea. Sci. Total Environ. 709:136144</ref> and the harvesting of seaweed<ref>Xiao, X., Agusti, S., Lin, F., Li, K., Pan, Y., Yu, Y., Zheng, Y., Wu, J. and Duarte, C.M. 2017. Nutrient removal from Chinese coastal waters by large-scale seaweed aquaculture. Scientific Reports 7: 46613 DOI: 10.1038/srep46613</ref>. The restoration of critical coastal habitats (seagrass meadows, coral reefs, oyster reefs, mangrove forests and salt-marshes) also contributes to remove nutrients, increase sequestration of organic matter in benthic sediment, and increase rates of denitrification<ref>Malone, T.C. and Newton, A. 2020. The Globalization of Cultural Eutrophication in the Coastal Ocean: Causes and Consequences. Front. Mar. Sci. 7:670</ref>.
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Local reduction of nutrient concentrations can be achieved by harvesting marine products that grow on nutrients and provide economic value (benefit from ecosystem goods and services) <ref>Burkholder, J. M., and Shumway, S.E. 2011. Bivalve shellfish aquaculture and eutrophication, in Shellfish Aquaculture and the Environment, ed. S.E. Shumway (Hoboken, NY: John Wiley & Sons, Inc.), 155–215</ref><ref>Petersen, J.K., Holmer, M., Termansen, M., Hasler, B. 2019. Nutrient extraction through bivalves. In: Smaal, A.C., Ferreira, J.G., Grant, J., Petersen, J.K., Strand, O. (Eds.), Goods and Services of Marine Bivalves. Springer, Cham, pp. 179–208</ref>. Examples are the harvesting of farmed mussels<ref>Kotta, J., Futter, M., Kaasik, A., Liversage, K., Rätsep, M., Barboza, F. R., et al. 2020. Cleaning up seas using blue growth initiatives: mussel farming for eutrophication control in the Baltic Sea. Sci. Total Environ. 709:136144</ref> and the harvesting of seaweed<ref>Xiao, X., Agusti, S., Lin, F., Li, K., Pan, Y., Yu, Y., Zheng, Y., Wu, J. and Duarte, C.M. 2017. Nutrient removal from Chinese coastal waters by large-scale seaweed aquaculture. Scientific Reports 7: 46613 DOI: 10.1038/srep46613</ref>. The restoration of critical coastal habitats (seagrass meadows, coral reefs, oyster reefs, mangrove forests and salt-marshes) also contributes to remove nutrients, increases sequestration of organic matter in benthic sediment, and increases rates of denitrification<ref>Malone, T.C. and Newton, A. 2020. The Globalization of Cultural Eutrophication in the Coastal Ocean: Causes and Consequences. Front. Mar. Sci. 7:670</ref>.
  
 
Certain measures may contribute to mitigate the impact of HABs (for a more detailed and complete overview see e.g. Berdalet et al., 2016<ref name=Ber16/> and Wells et al., 2020<ref> Wells, M.L., Karlson, B., Wulff, A., Kudela, R., Trick, C., Asnaghi, V., Berdalet, E., Cochlan, W.,. Davidson, K., De Rijcke, M., Dutkiewicz, S., Hallegraeff, G., Flynn, K.J., Legrand, C., Paerl, H., Slke, J., Suikkanen, S., Thompson, P. and Trainer, V.L. 2020. Future HAB science: Directions and challenges in a changing climate. Harmful Algae 91, 101632</ref>):
 
Certain measures may contribute to mitigate the impact of HABs (for a more detailed and complete overview see e.g. Berdalet et al., 2016<ref name=Ber16/> and Wells et al., 2020<ref> Wells, M.L., Karlson, B., Wulff, A., Kudela, R., Trick, C., Asnaghi, V., Berdalet, E., Cochlan, W.,. Davidson, K., De Rijcke, M., Dutkiewicz, S., Hallegraeff, G., Flynn, K.J., Legrand, C., Paerl, H., Slke, J., Suikkanen, S., Thompson, P. and Trainer, V.L. 2020. Future HAB science: Directions and challenges in a changing climate. Harmful Algae 91, 101632</ref>):
Line 63: Line 63:
  
 
Measures to eliminate harmful algae, for example through the use of viruses, grazers or biocides, encounter serious problems due to hazardous side effects<ref>Paerl, H.W. 2018. Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climate pressures. Toxins 10, 76; doi:10.3390/toxins10020076</ref>. That is why many countries have bans on such measures. Experiments in Korea to remove toxic algae through flocculation using clay particles have reported successful application without harmful side effects<ref>Yu, Z.M., Song, X.X., Cao, X.H. and Liu, Y., 2017. Mitigation of harmful algal blooms using modified clays: theory, mechanisms, and applications. Harmful Algae 69: 48–64</ref>.
 
Measures to eliminate harmful algae, for example through the use of viruses, grazers or biocides, encounter serious problems due to hazardous side effects<ref>Paerl, H.W. 2018. Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climate pressures. Toxins 10, 76; doi:10.3390/toxins10020076</ref>. That is why many countries have bans on such measures. Experiments in Korea to remove toxic algae through flocculation using clay particles have reported successful application without harmful side effects<ref>Yu, Z.M., Song, X.X., Cao, X.H. and Liu, Y., 2017. Mitigation of harmful algal blooms using modified clays: theory, mechanisms, and applications. Harmful Algae 69: 48–64</ref>.
−
Another, more holistic approach to toxic HAB mitigation experimented in Puget Sound (USA), is the restoration of coastal habitats with seagrass that harbor algicidal bacteria<ref>Inaba, N., Trainer, V.L., Onishi, Y., Ishii, K., Wyllie-Echeverria, S., Imai, I.and 2017. Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sounds, WA, USA. Harmful Algae 62: 136–147</ref><ref>Inaba, N., Trainer, V.L., Nagain, S., Kojima, S., Sakami, T., Takagi, S. and Imai, I. 2019. Dynamics of seagrass bed microbial communities used to control artificial Chattonella blooms: a microcosm study. Harmful Algae 84: 139–150</ref>.   
+
Another, more holistic approach to toxic HAB mitigation experimented in Puget Sound (USA), is the restoration of coastal habitats with seagrass that harbors algicidal bacteria<ref>Inaba, N., Trainer, V.L., Onishi, Y., Ishii, K., Wyllie-Echeverria, S., Imai, I.and 2017. Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sounds, WA, USA. Harmful Algae 62: 136–147</ref><ref>Inaba, N., Trainer, V.L., Nagain, S., Kojima, S., Sakami, T., Takagi, S. and Imai, I. 2019. Dynamics of seagrass bed microbial communities used to control artificial Chattonella blooms: a microcosm study. Harmful Algae 84: 139–150</ref>.   
  
  
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* [[Possible consequences of eutrophication]]
 
* [[Possible consequences of eutrophication]]
 
* [[ALGADEC - Detection of toxic algae with a semi-automated nucleic acid biosensor]]
 
* [[ALGADEC - Detection of toxic algae with a semi-automated nucleic acid biosensor]]
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* [[Marine Plankton]]
 
* [[Algal bloom dynamics]]
 
* [[Algal bloom dynamics]]
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* [[Algal bloom]]
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* [[Mariculture]]
 
* [[Eutrophication in coastal environments]]
 
* [[Eutrophication in coastal environments]]
 
* [[Real-time algae monitoring]]
 
* [[Real-time algae monitoring]]

Revision as of 16:27, 3 August 2021

Definition of Harmful Algal Bloom (HAB):
Harmful algal blooms or HABs are algal blooms composed of phytoplankton that naturally produce biotoxins. Harmful algal blooms (HABs) can occur in marine, estuarine, and fresh waters.
The term 'harmful algal bloom' is sometimes used to designate any phytoplankton bloom event that causes 'negative' impacts on the marine ecosystem, for example oxygen depletion or sunlight shading.
This is the common definition for Harmful Algal Bloom (HAB), other definitions can be discussed in the article


This article deals with toxic algal blooms: effects, environmental conditions, factors that promote HABs and management measures.


Effects of harmful algal blooms

The toxins produced by harmful algal blooms (HABs) have direct negative impacts on human health and on many marine organisms. Marine HABs further impact on other aspects of human wellbeing, including human commercial and recreational uses of the coastal and marine environments, such as fishing, aquaculture and tourism, and non-market, passive uses of the ocean, such as preferences for particular ecological states.

Most algal toxins are neurotoxins, which can affect the nervous, digestive, respiratory, hepatic, dermatological or cardiac systems. Consumption of toxins bio-accumulated in shellfish produces shellfish poisoning (PS) syndromes such as [1] Amnesic SP, Azaspirazid SP, Diarrhetic SP, Neurotoxic SP and Paralytic SP. Toxins in fish can produce Ciguatera Fish Poisoning.

Beach visitors can experience serious health problems when respiring aerosols containing algal biotoxins[2][3]. Toxic HABs have recently emerged as a potential risk for the contamination of drinking water supplied by desalination systems[4][5][6].


Socio-economic costs cannot easily be quantified, but they are considerable[7][1][8]. Estimates are in the order of several billon US$ annually up to about 8 billion US$, related to precautionary closure of mariculture farms, reduced attractiveness of beaches for coastal tourists and economic impacts of marine phycotoxins on human health.

The greatest direct effect of HABs concerns mariculture. Mariculture has experienced tremendous growth in recent decades and has become a food source on which much of the world's population depends. As the growth of mariculture is expected to continue, harmful algal blooms are an increasing threat. The paradox is that the waste from finfish farms itself promotes conditions for the development of HABs[9][10].


Conditions favouring the development of harmful algal blooms

HABs are natural phenomena, but these events can be favoured by anthropogenic pressures in coastal areas. It is not known exactly how toxin producing algae develop. What is known, however, is that most toxic algae belong to the class of flagellates and cyanobacteria. Environmental conditions favorable for the development of flagellates and cyanobacteria therefore create the greatest risk for the development of HABs. Among the algae of the diatom class (large plankton with silica cell wall) there are also toxic species, but these are rarer than among the flagellates. The following is known about the shift from conditions favorable for the development of diatoms to conditions favorable for the development of flagellates and cyanobacteria, thus promoting the occurrence of harmful algal blooms:

  1. Higher temperatures. The optimal growth of diatoms occurs at relatively low temperatures compared to flagellates and cyanobacteria[11]. This is consistent with experiments that show increasing occurrence of HABs with temperature[12]. Warmer waters are thought to also favour smaller-sized cells (less diatoms and more potentially harmful flagellates and cyanobacteria) as they are more efficient in harvesting light and nutrients and maintaining their position in the euphotic zoneCite error: Closing </ref> missing for <ref> tag.
  2. A high ratio of dissolved nitrogen N versus phosphorus P. This has several causes: (a) Very small cells, such as picocyanobacteria, have a lower requirement for P due to the smaller need for structural components in the cell[13]; (b) Many harmful dinoflagellates are mixotrophic [14][15], which means that they can ingest dissolved and particulate organic material and thus correct an imbalance in the stoichiometric N:P ratio[16][17][18]; (c) Harmful algae can release excess N via toxins [19]. Many cyanobacteria and marine dinoflagellate HABs are more toxic when N is in stoichiometric excess over P. In the dinoflagellate Alexandrium tamarense, saxitoxin production has been shown to increase by three- to fourfold under P deficiency[20]. Increasing N:P ratios in ecosystems therefore shift communities toward systems with trait dominance of higher optimal N:P ratios (higher P uptake affinity and decreasing N retention) which is a typical HAB trait[21].
  3. Increasing proportions of N in the form of ammonium and urea (CO(NH2)2). Causes: (a) Potentially harmful flagellates and cyanobacteria grow better on ammonium (NH4+) whereas diatoms prefer nitrate (NO3-)[22]; (b) Mixotrophic harmful dinoflagellates can use urea as food source[23].
  4. Enhancement of stratified conditions[24]. Causes for favouring potentially harmful flagellates and cyanobacteria over diatoms are: (a) Larger phytoplankton sinks more easily out of the photic zone, thus smaller plankton dominates [25]; (b) Many harmful dinoflagellates are mixotrophs which can swim to the pycnocline to capture organic prey[26].
  5. Reduction of the Si:N ratio. Diatoms require Si for growth; Si limitation favours non-Si species such as flagellates and cyanobacteria[27].


Causes for an increase in HABs

Although no quantitative estimates can be given, there is strong evidence that the occurrence of harmful algal blooms has increased during the past decades. The causes for an increase in HABs are related to the furtherance of the above mentioned conditions favorable to their development. Probable causes are[28]:

  1. Increase of nitrogen-rich effluents and atmospheric emissions to the sea. It has been estimated that the atmospheric deposition of nutrients in the ocean is now about 20-fold greater than the Redfield ratio for N:P. The main cause is the increasing use of fertilizers; in the period 1970-2000 the N-fertilizer use has increased much faster than the P-fertilizer use (see Fig. 1) [29]. Only about half of the fertilizer N is taken up by crops; the remainder is partly stored in the soil and partly emitted to the sea via runoff and the atmosphere. Other N-rich sources are the widespread and expanding fish farms, which release N mainly in chemically reduced form (e.g., ammonium, dissolved organic N, DON)[30]. The increase of the N:P ratio is further due to the more efficient reduction of P compared to N in sewage treatment plants and the reduction of P in laundry products.
  2. Fertilizer effluents and emissions produce a shift from nitrate to ammonium and urea, which favours HABs[19][23].
  3. Effect of river dams. Large fractions of the fluvial P load (about 43% of total dissolved P and reactive particulate P) and Si load (about 20% of dissolved Si and reactive particulate Si) are bound to sediments that are retained in upstream reservoirs, whereas about 90% of the total N load is unaffected[27][31]. This result in an increase in the N:P and N:Si ratios of riverine delivery to coastal areas following dam construction.
  4. Effects of climate change: (a) Rising seawater temperatures; (b) Intensification of sea water stratification; (c) Increase in peak river discharges and corresponding increase in nitrogen supply in coastal waters[32]; (d) Increase in nutrient concentrations associated with intensification of upwelling events[33].
  5. Spreading of harmful algae species across the oceans by increased transport of algae with ship ballast water[1].


Fig. 1. N and P content of global fertilizer use. After Glibert and Burford (2017[34]) and FAO (2019[35]).


Measures for reducing the risk of HABs

The factors that promote the occurrence of HABs are expected to become more important in the future. This holds in the first place for global warming and for eutrophication, in particular the nitrogen component of eutrophication. Efforts to combat harmful algal blooms are vital, but simple solutions do not exist. It is widely recognized that action is needed to halt global climate change and to reduce nitrogen emissions from agriculture. To this end, agreements have been made and initiatives have been developed at various administrative levels. Important international frameworks have been set up for climate policy that will eventually reverse the trend of global warming. A comparable encompassing agreement has not yet been established for agricultural emissions, although in Europe the Nitrates Directive has been in force since 1991. This directive has contributed to a reduction in N emissions from European agriculture[36] - however, without special focus on the nitrate: ammonium ratio of the emissions.

Local reduction of nutrient concentrations can be achieved by harvesting marine products that grow on nutrients and provide economic value (benefit from ecosystem goods and services) [37][38]. Examples are the harvesting of farmed mussels[39] and the harvesting of seaweed[40]. The restoration of critical coastal habitats (seagrass meadows, coral reefs, oyster reefs, mangrove forests and salt-marshes) also contributes to remove nutrients, increases sequestration of organic matter in benthic sediment, and increases rates of denitrification[41].

Certain measures may contribute to mitigate the impact of HABs (for a more detailed and complete overview see e.g. Berdalet et al., 2016[1] and Wells et al., 2020[42]):

  • Development and implementation of new efficient techniques for monitoring HABs and biotoxins and for monitoring marine conditions that are favorable for the development of HABs, in order to improve early warning;
  • Management measures for aquaculture to reduce HAB development, for example by timing the harvest, by enhanced flushing and aeration or by relocation to offshore areas where excess N concentrations are less likely to build up;
  • Furthering understanding of fundamental aspects of HAB species in terms of toxin production, life cycles and interactions with bacteria in order to develop better targeted measures.

Measures to eliminate harmful algae, for example through the use of viruses, grazers or biocides, encounter serious problems due to hazardous side effects[43]. That is why many countries have bans on such measures. Experiments in Korea to remove toxic algae through flocculation using clay particles have reported successful application without harmful side effects[44]. Another, more holistic approach to toxic HAB mitigation experimented in Puget Sound (USA), is the restoration of coastal habitats with seagrass that harbors algicidal bacteria[45][46].


Useful links

Global Harmful Algal Blooms

Related articles


References

  1. ↑ 1.0 1.1 1.2 1.3 Berdalet, E., Fleming, L.E., Gowen, R., Davidson, K., Hess, P., Backer, L.C., Moore, S.K., Hoagland, P. and Enevoldsen, H. 2016. Marine harmful algal blooms, human health and wellbeing: challenges and opportunities in the 21st century. J. Mar. Biol. Assoc. U.K. 96: 61–91
  2. ↑ Fleming L.E., Kirkpatrick B., Backer L.C., Walsh C.J., Nierenberg K., Clark J., Reich A., Hollenbeck J., Benson J., Cheng Y.S., Naar J., Pierce R., Bourdelais A.J., Abraham W.M., Kirkpatrick G., Zaias J., Wanner A., Mendes E., Shalat S., Hoagland P., Stephan W., Bean J., Watkins S., Clarke T., Byrne M. and Baden D.G. 2011. Review of Florida red tide and human health effects. Harmful Algae 20: 224–233
  3. ↑ Berdalet E., Vila M. and Abos-Herrandiz, R. 2015. Expansion of the benthic dinoflagellate Ostreopsis with climate change: health risks assessment and policy strategies for management. Harmful Algal Blooms and Climate Change Scientific Symposium. Goteborg, Sweden, 19–22 May 2015
  4. ↑ Seubert, E.L., Trussell, S., Eagleton, J., Schnetzer, A., Cetinic, I., Lauri, P., Jones, B.H. and Caron, D.A. 2012. Algal toxins and reverse osmosis desalination operations: laboratory bench testing and field monitoring of domoic acid, saxitoxin, brevetoxin and okadaic acid. Water Research 46: 6563–6573
  5. ↑ Berman, T. 2013. Transparent exopolymer particles as critical agents in aquatic biofilm formation: implications for desalination and water treatment, Desalination and Water Treatment 51: 4-6
  6. ↑ Flemming, H.C. and Wingender, J. 2001. Relevance of microbial extracellular polymeric substances (EPSs)--Part I: Structural and ecological aspects. Water Sci Technol. 43(6): 1-8
  7. ↑ Hoagland P. and Scatasta S. (2006) The economic effects of harmful algal blooms. In Graneli E. and Turner J.T. (eds) Ecology of harmful algae. New York, NY: Springer-Verlag, pp. 391–402
  8. ↑ Ross Brown, A., Lilley, M., Shutler, J., Lowe, C., Artioli, Y, Torres, R., Berdalet, E. and Tyler, C.R. 2019. Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries. Rev. Aquacult. 1–26
  9. ↑ Anderson, D. 2012. HABs in a changing world: a perspective on harmful algal blooms, their impacts, and research and management in a dynamic era of climactic and environmental change. Harmful Algae 2012 (2012). 2014 ; 2012: 3–17 PMID: 26640829; PMCID: PMC4667985
  10. ↑ Strain, P. M., and Hargrave, B. T. 2005. Salmon aquaculture, nutrient fluxes and ecosystem processes in Southwestern New Brunswick, in Environmental Effects of Marine Finfish Aquaculture, Handbook of Environmental Chemistry, ed. B. T. Hargrave (Berlin: Springer): 29–57
  11. ↑ Anderson, N.J. 2000. Diatoms, temperature and climate change. Eur. J. Phycol. 35: 307–314
  12. ↑ Paerl, H.W. and Scott, J.T. 2010. Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environ. Sci. Technol. 44: 7756–7758
  13. ↑ Finkel, Z.V., J. Beardall, K.J. Flynn, A. Quiqq, T.A.V. Rees, and J.A. Raven. 2010. Phytoplankton in a changing world: Cell size and elemental stoichiometry. Journal of Plankton Research 32:119–137
  14. ↑ Mitra, A. and Flynn, K.J. 2010. Modelling mixotrophy in harmful algal blooms: more or less the sum of the parts? J. Mar. Syst. 83: 58–169
  15. ↑ Stoecker, D., Tillmann, U. and Graneli, E. 2006. Phagotrophy in harmful algae. In: Graneli, E. and Turner, J. (eds) Ecology of Harmful Algae, Series: Ecological Studies, Vol. 189, Springer Verlag, Heidelberg, pp 177–187
  16. ↑ Burkholder, J.M., Glibert, P.M. and Skelton, H. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8: 77–93
  17. ↑ Jeong, H.J., Yoo, Y.D., Kim, J.S., Seong, K.A., Kang, N.S. and Kim, T.H., 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45: 65–91
  18. ↑ Flynn, K.J., Stoecker, D.K., Mitra, A., Raven, J.A., Glibert, P.M., Hansen, P.J., Graneli, E. and Burkholder, J.M. 2013. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J. Plankt. Res 35: 3–11
  19. ↑ 19.0 19.1 Glibert, P.M., Wilkerson, F.P., Dugdale, R.C., Raven, J.A., Dupont, C., Leavitt, P.R., Parker, A.E., Burkholder, J.M. and 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
  20. ↑ Graneli, E., and Flynn, K.J. 2006. Chemical and physical factors influencing toxin content. Pp. 229–241 in Ecology of Harmful Algae. E. Graneli, and J.T. Turner, eds, Springer, Heidelberg, Germany
  21. ↑ Meunier, C.L., Boersma, M., El-Sabaawi, R., Halvorson, H.M., Herstoff, E.M., Van de Waal, D.B., Vogt, R.J. and Litchman, E. 2017. From elements to function: toward unifying ecological stoichiometry and trait-based ecology. Front. Environ. Sci 5, 18
  22. ↑ Glibert, P.M. 2017. Eutrophication, harmful algae and biodiversity - challenging paradigms in a world of complex nutrient changes. Mar. Poll. Bull. 124: 591–606
  23. ↑ 23.0 23.1 Glibert, P.M., Manager, R., Sobota, D.J., Bouwman, L. 2014. The Haber-Bosch-Harmful algal bloom (HB-HAB) link. Environ. Res. Lett. 9, 105001
  24. ↑ Telesh, I., Schubert, H. and Skarlato, S. 2021. Abiotic stability promotes dinoflagellate blooms in marine coastal ecosystems. Estuarine, Coastal and Shelf Science 251, 107239
  25. ↑ Winder, M., Reuter, J.E. and Schladow, S.G. 2009. Lake warming favours small-sized plankton diatom species. Proc. Roy. Soc B 276: 427–435
  26. ↑ Stoecker, D.K., Hansen, P.J., Caron, D.A. and Mitra, A. 2017. Mixotrophy in the marine plankton. Ann. Rev. Mar. Sci. 9: 311–335
  27. ↑ 27.0 27.1 Maavara, T., Dürr, H.H. and Van Cappellen, P. 2014. Worldwide retention of nutrient silicon by river damming: from sparse data set to global estimate. Glob. Biogeochem. Cycl. 28: 842–855
  28. ↑ Glibert, P.M. 2020. Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae 91, 101583
  29. ↑ Penuelas, J., Poulter, B., Sardans, J., Ciais, P., van der Velde, M., Bopp, L., et al. 2013. Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4: 2934
  30. ↑ Bouwman, A.F., Beusen, A.H.W., Glibert, P.M., Overbeck, C., Pawlowski, M., Silveiva, J.H., Mulsow, S., Yu, R. and Zhou, M.J. 2013. Mariculture: significant and expanding cause of coastal nutrient enrichment. Environ. Res. Lett. 8, 044026
  31. ↑ Maavara, T., Parsons, C.T., Ridenour, C., Stojanovic, S., Dürr, H.H., Powley, H.R. and Van Cappellen, P. 2015. Global phosphorus retention by river damming. Proc. Natl. Acad. Sci. U. S. A. 112, 15603–15608
  32. ↑ Howarth, R.W., Swaney, D.P., Boyer, E.W., Marino, R., Jaworski, N. and Goodale, C. 2006. The influence of climate on average nitrogen export from large watersheds in the Northeastern United States. Biogeochemistry 79: 163–186
  33. ↑ Goes, J.I., Thoppil, P.G., Gomes, H.D.R. and Fasullo, J.T. 2005. Warming of the Eurasian landmass is making the Arabian Sea more productive. Science 308: 545–547
  34. ↑ Glibert, P.M. and Burford, M.A. 2017. Globally changing nutrient loads and harmful algal blooms: Recent advances, new paradigms, and continuing challenges. Oceanography 30: 58–69
  35. ↑ FAO. 2019. World fertilizer trends and outlook to 2022. FAO, Rome
  36. ↑ Velthof G.L., Lesschen, J.P., Webb, J., Pietrzak, S., Miatkowski, Z., Pinto, M., Kros, J. and Oenema, O. 2014.The impact of the Nitrates Directive on nitrogen emissions from agriculture in the EU-27during 2000–2008. Science of the Total Environment 468–469: 1225–1233
  37. ↑ Burkholder, J. M., and Shumway, S.E. 2011. Bivalve shellfish aquaculture and eutrophication, in Shellfish Aquaculture and the Environment, ed. S.E. Shumway (Hoboken, NY: John Wiley & Sons, Inc.), 155–215
  38. ↑ Petersen, J.K., Holmer, M., Termansen, M., Hasler, B. 2019. Nutrient extraction through bivalves. In: Smaal, A.C., Ferreira, J.G., Grant, J., Petersen, J.K., Strand, O. (Eds.), Goods and Services of Marine Bivalves. Springer, Cham, pp. 179–208
  39. ↑ Kotta, J., Futter, M., Kaasik, A., Liversage, K., Rätsep, M., Barboza, F. R., et al. 2020. Cleaning up seas using blue growth initiatives: mussel farming for eutrophication control in the Baltic Sea. Sci. Total Environ. 709:136144
  40. ↑ Xiao, X., Agusti, S., Lin, F., Li, K., Pan, Y., Yu, Y., Zheng, Y., Wu, J. and Duarte, C.M. 2017. Nutrient removal from Chinese coastal waters by large-scale seaweed aquaculture. Scientific Reports 7: 46613 DOI: 10.1038/srep46613
  41. ↑ Malone, T.C. and Newton, A. 2020. The Globalization of Cultural Eutrophication in the Coastal Ocean: Causes and Consequences. Front. Mar. Sci. 7:670
  42. ↑ Wells, M.L., Karlson, B., Wulff, A., Kudela, R., Trick, C., Asnaghi, V., Berdalet, E., Cochlan, W.,. Davidson, K., De Rijcke, M., Dutkiewicz, S., Hallegraeff, G., Flynn, K.J., Legrand, C., Paerl, H., Slke, J., Suikkanen, S., Thompson, P. and Trainer, V.L. 2020. Future HAB science: Directions and challenges in a changing climate. Harmful Algae 91, 101632
  43. ↑ Paerl, H.W. 2018. Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climate pressures. Toxins 10, 76; doi:10.3390/toxins10020076
  44. ↑ Yu, Z.M., Song, X.X., Cao, X.H. and Liu, Y., 2017. Mitigation of harmful algal blooms using modified clays: theory, mechanisms, and applications. Harmful Algae 69: 48–64
  45. ↑ Inaba, N., Trainer, V.L., Onishi, Y., Ishii, K., Wyllie-Echeverria, S., Imai, I.and 2017. Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sounds, WA, USA. Harmful Algae 62: 136–147
  46. ↑ Inaba, N., Trainer, V.L., Nagain, S., Kojima, S., Sakami, T., Takagi, S. and Imai, I. 2019. Dynamics of seagrass bed microbial communities used to control artificial Chattonella blooms: a microcosm study. Harmful Algae 84: 139–150


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