Difference between revisions of "Eutrophication"

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Eutrophication is an important process involving enrichment of water by excess nutrients.  It can cause serious problems in the coastal zone through disturbance of ecological balances and fisheries, and through interference with recreational activities and quality of life. 
 
  
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{{Definition
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|title=
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Eutrophication
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|definition = (1) An increase in the supply of organic matter (Nixon, 1995<ref>Nixon, S. W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41: 199–219</ref>) <br>
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(2) A condition in an aquatic ecosystem where high nutrient concentrations stimulate growth of [[algae]] which leads to imbalanced functioning of the system (HELCOM 2006<ref>HELCOM 2006[http://www.helcom.fi/environment2/eutrophication/en_GB/front/]</ref>)<br>
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(3) The enrichment of water by [[nutrient]]s, especially nitrogen and/or phosphorus and organic matter, causing an increased growth of algae and higher forms of plant life to produce an adverse deviation in structure, function and stability of organisms present in the water and to the quality of water concerned, compared to reference conditions (Andersen et al. 2006<ref>Andersen, J. H., Schlüter, L. and Ærtebjerg, G. 2006. Coastal eutrophication: recent developments in definitions and implications for monitoring strategies. J. Plankton Res 28(7): 621-628</ref>)<br>
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(4) The enrichment of water by nutrients causing an accelerated growth of algae and higher forms of plant life to produce an undesirable disturbance to the balance of organisms present in the water and to the quality of the water concerned” (OSPAR 2003<ref>OSPAR, 2003. In: Strategies of the OSPAR commission for the protection of the marine environment of the north-east Atlantic (reference number: 2003e21)</ref>
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}}
  
==What is eutrophication about?==
 
[[image:Baltic.jpg|thumb|right|Cyanobacteria bloom, Western Baltic, 1997]]
 
*It’s about '''increased productivity''' (conversion of light and carbon dioxide into living organic matter – a process being limited by ''nitrogen'' and/or ''phosphorus'') and unacceptable ecological effects as algal blooms, oxygen depletion, kills of benthic animals and fish
 
  
*It’s caused by '''increased inputs''' of nutrients from point sources, activities in the upstream catchment (''e.g.'' losses from agriculture) and atmospheric deposition.
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Eutrophication occurs when a limiting factor on the rate of growth and production of primary producers is released, most frequently via an input of inorganic or organic nutrients (Howarth 1988<ref>Howarth, R.W. 1988. Nutrient limitation of net primary production in marine ecosystems. Annual Rev. Ecol. Syst. 19: 89–110</ref>). High [[primary production]] boosted by eutrophication usually leads to oxygen depletion caused by decay of organic matter.
  
  
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==Nutrients involved in eutrophication==
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====Nutrients needed in large quantities====
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*Nitrogen (<math>N</math>) is often a limiting nutrient to growth. Most common reactive form is dissolved inorganic nitrogen (DIN) found in marine waters as nitrate (<math>NO_3^-</math>), nitrite (<math>NO_2^-</math>) and ammonium (<math>NH_4^+</math>). Nitrogen also occurs in the largely refractory form of dissolved organic matter (DOM) as dissolved organic nitrogen (DON). Small amounts of nitrogen occur in the not directly usable form of particulate organic matter (POM).
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*Phosphorous (<math>P</math>) is often a limiting nutrient to growth. Most common reactive form is dissolved inorganic phosphorus (DIP) found as phosphate (<math>PO_4^{3-}</math>). Phosphorus also occurs in the largely refractory form of dissolved organic matter (DOM) as dissolved organic phosphorus (DOP). Small amounts of phosphorus occur in the not directly usable form of particulate organic matter (POM).
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*Potassium (<math>K</math>)
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*Calcium (<math>Ca</math>)
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*Magnesium (<math>Mg</math>)
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*Sulfur (<math>S</math>)
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* Silicium (<math>Si</math>), mainly as silicic acid <math>Si(OH)_4</math> can be a limiting nutrient for diatoms
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====Nutrients needed in trace amounts====
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*Iron (<math>Fe</math>) can be a limiting nutrient
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*Boron (<math>B</math>)
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*Chlorine (<math>Cl</math>)
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*Manganese (<math>Mn</math>)
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*Zinc (<math>Zn</math>) can be a limiting nutrient
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*Copper (<math>Cu</math>)
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*Nickel (<math>Ni</math>)
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*Molybdenum (<math>Mo</math>)
  
===What are we really talking about?===
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==Eutrophication indicators==
;Eutrophication : “eu” = “well” or “good”
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There are no widely applicable indicators of eutrophication due to the high variation in natural
:“trope” = “nourishment”
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conditions and the interaction of multiple factors influencing eutrophication. Often Chlorophyll a (<math>Cl \, a</math>) is used as indicator of eutrophication, as a proxy for phytoplankton biomass. However, the drawback of using of <math>Cl \, a</math> as an indicator is that there can be no increase in <math>Cl \, a</math> after nutrient concentrations have exceeded the threshold beyond which other factors (e.g. light, grazing) are limiting. Additionally, <math>Cl \, a</math> measures only changes in the abundance of primary producers and cannot indicate any changes in community composition that may occur simultaneously (Jessen et al. 2015<ref>Jessen, C., Bednarz, V.N., Rix, L., Teichberg, M. and Wild, C. 2015. Marine Eutrophication. In: Armon, R., Hänninen, O. (eds) Environmental Indicators. Springer, Dordrecht</ref>).
  
  
But is “eutrophication” good?
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==Articles related to eutrophication==
*In general: NO … it is actually ”bad” …
 
*Too many nutrients in wrong places may cause problems and result in changes in structure, function and stability of the marine ecosystems
 
  
*Eutrophication is ”too much of a good thing”
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===Eutrophication processes===
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* [[Eutrophication in coastal environments]]
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* [[What causes eutrophication?]]
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* [[Nutrient conversion in the marine environment]]
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* [[Which resource limits coastal phytoplankton growth/ abundance: underwater light or nutrients?]]
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* [[Marine microorganisms]]
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* [[Marine Plankton]]
  
==Some definitions:==
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===Eutrophication impacts===
[[image:German Bight.jpg|thumb|right|Noctiluca milaris bloom, German Bight, 2000]]
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* [[Threats to the coastal zone]]
;Eutrophication : An increase in the supply of organic matter<ref name="NIXON">Nixon, S. W. (1995) Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia, 41, 199–219.[ISI]</ref>
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* [[Coastal pollution and impacts]]
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* [[Possible consequences of eutrophication]]
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* [[Algal bloom]]
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* [[Algal bloom dynamics]]
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* [[Case studies eutrophication]]
  
: A condition in an aquatic ecosystem where high nutrient concentrations stimulate growth of algae which leads to imbalanced functioning of the system<ref> HELCOM webpage, 2006 [http://www.helcom.fi/environment2/eutrophication/en_GB/front/]</ref>.
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===Eutrophication monitoring===
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* [[In situ monitoring of eutrophication]]
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* [[Plankton remote sensing]]
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* [[Plankton remote sensing North Sea]]
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* [[Real-time algae monitoring]]
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* [[Optical measurements in coastal waters]]
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* [[Nutrient analysers]]
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* [[Differentiation of major algal groups by optical absorption signatures]]
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* [[Sampling tools for the marine environment]]
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* [[FerryBox - Continuous and automatic water quality observations along transects]]
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* [[Detecting the unknown - novelty detection of exceptional water reflectance spectra]]
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* [[The Baltic Algae Watch System - a remote sensing application for monitoring cyanobacterial blooms in the Baltic Sea]]
  
;Alternative proposal : The enrichment of water by [[nutrients]], especially nitrogen and/or phosphorus and organic matter, causing an increased growth of algae and higher forms of plant life to produce an unacceptable deviation in structure, function and stability of organisms present in the water and to the quality of water concerned, compared to reference conditions<ref>Andersen, J. H., Schlüter, L. and Ærtebjerg, G. (2006) Coastal eutrophication: recent developments in definitions and implications for monitoring strategies. J. Plankton Res. 28(7): 621-628.</ref>
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===Eutrophication modelling===
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* [[Coupled hydrodynamic - water quality - ecological modelling]]
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* [[Nutrient loading of coastal waters]]
  
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===Eutrophication policy===
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* [[OSPAR and eutrophication]]
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* [[OSPAR eutrophication assessment]]
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* [[European policy on eutrophication: introduction]]
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* [[European Context of Nutrient Dynamics]]
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* [[Eutrophication related monitoring tasks and WFD for coastal waters in Greece]]
  
  
==Effects of Eutrophication==
 
The different processes and effects of coastal eutrophication are well documented<ref>Cloern, J. (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser., 210, 223–253.[ISI]</ref> <ref>Conley, D. J., Markager, S., Andersen, J. et al. (2002) Coastal eutrophication and the Danish National Aquatic Monitoring and Assessment Program. Estuaries, 25, 706–719.[Medline]</ref> <ref>Rönnberg, C. and Bonsdorff, E. (2004) Baltic Sea eutrophication: area-specific ecological consequences. Hydrobiologia, 514, 227–241.[CrossRef][ISI]</ref>. and it has been considered as one of the biggest threats to marinne ecosystem health for decades<ref>Ryther and Dunstan, 1971</ref> <ref name="NIXON"/> <ref>Bachmann, R. W., Cloern, J. E., Heckey, R. E. et al. (eds) (2006) Eutrophication of freshwater and marine ecosystems. Limnol. Oceanogr., 51 (1, part 2), 351–800.</ref>.
 
 
[[Image:eutrophicationflow.jpg|600px|centre|Source: HELCOM, 2006 <ref name="HELCOM">HELCOM, (2006) Andersen, J (DHI) and Pawlak, J (MEC), Nutrients and Eutrophication in the Baltic Sea – Effects, Causes, Solutions. Baltic Sea Parliamentary Conference. </ref>
 
]]
 
 
Effects of eutrophication on marine [[ecosystems]] are well known<ref name="HELCOM"/>:
 
*algal blooms resulting in green water
 
*reduced depth distribution of submerged aquatic vegetation
 
*increased growth of nuisance macroalgae
 
*increased sedimentation, increased oxygen consumption
 
*oxygen depletion in bottom water, and
 
*sometimes dead benthic animals and fish.
 
 
 
[[image:koncept.jpg|200px|frame|centre|Eutrophication schematic. Source:HELCOM, 2006 <ref name="HELCOM"/>]]
 
 
Major effects include structure and function changes in the entire marine ecosystem and a reduction in stability. Responses to increased nutrient inputs<ref name="HELCOM"/>:
 
#Corresponding increase in nutrient concentrations
 
#Change in ratio between dissolved nitrogen and phosphorus in the water: DIN:DIP ratio. Optimal is 16:1 – called the Redfield ratio.
 
*significantly lower: potential nitrogen limitation;
 
*higher N/P ratio: phosphorus limitation of phytoplankton primary production
 
 
'''Primary production:'''
 
*usually limited by availability of light and nutrients
 
**nutrient enrichment increase phytoplankton primary production
 
**which increases biomass -- decrease light penetration through water column
 
**(light penetration measured by Secchi depth)
 
*Decreased Secchi depth can reduce colonization depth of macroalgae and seagrasses
 
 
'''Responses to nutrient enrichment (pelagic ecosystems) involve a gradual change towards<ref name="HELCOM"/>:'''
 
#Increased planktonic primary production compared to benthic production
 
#Dominance of microbial food webs over linear planktonic food chains
 
#Dominance of non-siliceous phytoplankton species over diatom species
 
#Dominance of gelatinous zooplankton (jellyfish) over crustacean zooplankton
 
 
'''Eutrophication issues<ref name="HELCOM"/>:'''
 
#Causative factors
 
*inputs, elevated nutrient concentrations, Redfield ratio changes
 
#Direct effects
 
*primary producers, namely:
 
**Phytoplankton
 
**Submerged aquatic vegetation
 
#Indirect effects (secondary effects)
 
*related to:
 
**Zooplankton
 
**Fish
 
**Invertebrate benthic fauna (animals living on seafloor)
 
 
 
===Phytoplankton===
 
*are at base of pelagic food webs in aquatic systems
 
*generation times: from less that a few days
 
*respond rapidly to nutrient concentration changes
 
Often quantified in terms of:
 
#Primary production
 
#Biomass (chlorophyll-a concentration, or carbon biomass)
 
#Bloom frequency
 
 
===Submerged aquatic vegetation:===
 
Are affected by eutrophication through<ref name="HELCOM"/>:
 
#Reduced light penetration and shadowing effects from phytoplankton can reduce the depth distribution, biomass, composition and species diversity
 
#increased growth of filamentous and short lived nuisance macroalgae at cost of long lived species lead to a change in structure of macroalgae community with reduced diversity
 
*seagrass meadows and perennial macroalgae are important nursery areas for coastal fish populations
 
*short-lived (annual) nuisance macroalgae favoured by large nutrient inputs
 
 
===Oxygen depletion<ref name="HELCOM"/>:===
 
*“hypoxia”: a common effect of eutrophication in bottom waters
 
May be:
 
#Episodic
 
#Occur annually (most common in summer/autumn)
 
#Persistent
 
#Periodic in the coastal zone
 
*Lethally low oxygen concentrations depend on the species.
 
*Fish and crustaceans have higher oxygen requirements; other speices lower.
 
*Hypoxic and anoxic (no oxygen) conditions may results in formation and releast of hydrogen sulphide (H<sub>2</sub>S) – lethal to organisms
 
*Anoxic periods cause release of phophorus from sediments. Dissolved inorganic phosphorus (DIP)
 
*Ammonium released under hypoxic conditions
 
*DIP and ammonium in water column can enhance algal blooms
 
*Predicted effect of global warming is to increase hypoxia with increased temperature. A 4 degree temperature increase is projected to results in a doubling of hypoxia in some parts of North Sea.
 
*eg eelgrass responds to low oxygen concentrations, and dies off (often in combination with high temperatures)
 
 
===Invertebrate benthic fauna<ref name="HELCOM"/>:===
 
*can cope with oxygen depletion to varying degrees (days – month)
 
*if O<sub>2</sub> drops below zero and H<sub>2</sub>S is released all organisms killed immediately
 
*mobile benthic invertebrates in sediment move to surface when O<sub>2</sub> decreases
 
**increased catches of fish and crustaceans
 
*Difficult to predict when animals will return after eutrophication events
 
*Size of area plays a factor: small areas are recolonised and re-established more quickly
 
 
 
===Climate change===
 
*seas are important in element cycling – carbon and nitrogen cycle; phosphorus and silicate cycle
 
*ocean still takes up more carbon than it releases – depositing some in sediments
 
 
==European Coastal Areas==
 
The main source of nitrogen to European coastal waters is agricultural runoff discharged into the sea via rivers, identified as originating from sources of ammonia evaporation in animal husbandry and partly from fossil fuel combustion in traffic, industry and households<ref name="ECW">Ærtebjerg, G. et al., Eutrophication in Europe’s Coastal Waters. Topic Report No 7/2001. European Environment Agency.  [http://reports.eea.europa.eu/topic_report_2001_7/en]</ref>. For phosphorus the major sources are treated and untreated discharges to the sea from households and industry as well as soil erosion<ref name="ECW"/>.
 
 
===Baltic Sea in focus===
 
Eutrophication seriously affects the Baltic sea marine environment, resulting in algal blooms, reduced water clarity, oxygen reduction and death of bottom animals. The causes behind this are well known<ref name="HELCOM"/>: discharges, losses and emissions of nitrogen and phosphorus to the aquatic environment. Reductions of discharges from municipal wastewater treatment plants and industries have been in focus for many years as have losses and emissions of nitrogen compounds from agriculture and traffic.
 
 
====Causes in Baltic Sea====
 
Human-mediated nutrient enrichment<ref name="HELCOM"/>:
 
For Baltic Sea, input of nutrients can be in form of
 
#Direct inputs from point sources (sewage treatment plants, industries
 
#Atmospheric deposition
 
#Riverine inputs (from activities in the catchment: eg point sources, agricultural losses, atmospheric deposition, natural background losses (natural erosion and leakage of nutrients from areas without much human activities) and stream, river and lake retention)
 
 
'''Waterborne:'''
 
*Agriculture forestry, scattered dwellings, municipanlities, industries, natural background losses.
 
 
'''Airborne:'''
 
*Nitrogen compounds emitted to atmosphere:
 
*Nitrogen oxides: road transportation, energy combustion, shipping
 
*Ammonia emissions: mostly from agriculture.
 
*Distant sources
 
 
'''Role of agriculture:'''
 
*main source in Baltic Sea is agricultural discharge via rivers, from:
 
#Soil cultivation
 
#Fertiliser use
 
#Use of manure
 
#Intensive and uncontrolled agriculture
 
 
 
====Aspects of Eutrophication problem in the Baltic sea<ref name="HELCOM"/>====
 
*excessive phytoplankton blooms are major problem – especially of blue-green algae
 
*summertime algal blooms in most parts of Gulf of Finland, Gulf of Riga, the Baltic Proper and south-western parts of Baltic Sea
 
*problems:
 
**bathing people can hardly see their feet
 
**blue-green algae potentially toxic to humans and animals
 
**large mats of drifting algae deposited along shores and decay
 
*increased phytoplankton abundance results in reduced water clarity and reduced light penetration through water column to sea floor
 
 
====Baltic Sea Solutions====
 
The following steps are suggested<ref>HEL</ref>
 
#Establish overall goals and target values
 
#Implement relevant measures directly linked to fulfillment of these overall goals and targets
 
#Carry out monitoring
 
#Conduct assessments
 
#Evaluate whether the goals and targets have been fulfilled or not
 
 
'''Main drivers:'''
 
*European Directives
 
*Decisions and recommendations adopted by HELCOM
 
*National action plans
 
 
==Solutions==
 
Nutrient inputs must be reduced to levels that do not put at risk target values for mitigation of eutrophication. Integrated management strategies should enable characterization of all pressures on water bodies in order to develop a coherent approach to deal with the pressures in a cost effective manner<ref name="HELCOM"/>.
 
 
==EU Directives:==
 
*[http://ec.europa.eu/environment/water/water-urbanwaste/directiv.html EC Urban Waster Water Treatment Directive]
 
*[http://ec.europa.eu/environment/water/water-nitrates/directiv.html EC Nitrates Directive]
 
*[http://ec.europa.eu/environment/water/water-framework/index_en.html EU Water Framework Directive]
 
*[http://ec.europa.eu/environment/water/marine.htm Marine Strategy Directive]
 
 
==See also==
 
Wikipedia: [http://en.wikipedia.org/wiki/Eutrophication Eutrophication article]
 
 
==External links==
 
*[http://www.BSPC.net Baltic Sea Parlimentary Conference ]
 
*[http://www.bernet.org/wm125051 BERNET:] Baltic Eutrophication Regional Network
 
*[http://www.BONUSportal.org BONUS] for the future of the Baltic Sea
 
*[http://www.EEA.europa.eu European Environment Agency ]
 
*[http://www.HELCOM.fi HELCOM ]
 
*HELCOM Indicator fact sheets: [http://www.helcom.fi/environment2/ifs/ifs2005/en_GB/inflow water exchange], [http://www.helcom.fi/environment2/ifs/ifs2005/en_GB/winternutriets winter nutrient concentrations], [http://www.helcom.fi/environment2/ifs/ifs2005/en_GB/transparency water clarity], [http://www.helcom.fi/environment2/ifs/ifs2005/en_GB/blooms algal blooms], [http://www.helcom.fi/environment2/ifs/ifs2005/Chlorophyll-a/en_GB/chlorophyll chlorophyll-a concentrations], [http://www.helcom.fi/environment2/ifs/ifs2005/en_GB/oxygen_deepbasins hydrography and oxygen in the deep basins]
 
*[http://www.MARE.su.se MARE] Research program on Baltic Sea environmental issues
 
*[http://www.dmu.dk/International/Water/ National Environment Research Institute (DK) Aquatic page]
 
*[http://www2.dmu.dk/1_Viden/2_Miljoe-tilstand/3_vand/4_eutrophication/definition.htm Nutrients and Eutrophication in Danish Marine Waters]
 
*[http://www.OSPAR.org OSPAR] For the protection of the marine environment of the north-east Atlantic
 
*[http://www.waterforecast.com/defaultUK.asp The Water Forecast]
 
*[http://www.panda.org/about_wwf/where_we_work/europe/what_we_do/baltics/our_work/index.cfm WWF Baltic Ecoregion Programme]
 
  
 
==References==
 
==References==
 
<references/>
 
<references/>
  
 
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[[Category:Eutrophication]]
 
 
Authorship
 
''02/01/2007, Jesper Andersen (jha@dhigroup.dk), DHI Water Environment Health.''
 
 
 
(Caitlin 09:31, 18 January 2007 (Romance Standard Time))
 

Latest revision as of 12:31, 11 November 2024

Definition of Eutrophication:
(1) An increase in the supply of organic matter (Nixon, 1995[1])

(2) A condition in an aquatic ecosystem where high nutrient concentrations stimulate growth of algae which leads to imbalanced functioning of the system (HELCOM 2006[2])
(3) The enrichment of water by nutrients, especially nitrogen and/or phosphorus and organic matter, causing an increased growth of algae and higher forms of plant life to produce an adverse deviation in structure, function and stability of organisms present in the water and to the quality of water concerned, compared to reference conditions (Andersen et al. 2006[3])

(4) The enrichment of water by nutrients causing an accelerated growth of algae and higher forms of plant life to produce an undesirable disturbance to the balance of organisms present in the water and to the quality of the water concerned” (OSPAR 2003[4]
This is the common definition for Eutrophication, other definitions can be discussed in the article


Eutrophication occurs when a limiting factor on the rate of growth and production of primary producers is released, most frequently via an input of inorganic or organic nutrients (Howarth 1988[5]). High primary production boosted by eutrophication usually leads to oxygen depletion caused by decay of organic matter.


Nutrients involved in eutrophication

Nutrients needed in large quantities

  • Nitrogen ([math]N[/math]) is often a limiting nutrient to growth. Most common reactive form is dissolved inorganic nitrogen (DIN) found in marine waters as nitrate ([math]NO_3^-[/math]), nitrite ([math]NO_2^-[/math]) and ammonium ([math]NH_4^+[/math]). Nitrogen also occurs in the largely refractory form of dissolved organic matter (DOM) as dissolved organic nitrogen (DON). Small amounts of nitrogen occur in the not directly usable form of particulate organic matter (POM).
  • Phosphorous ([math]P[/math]) is often a limiting nutrient to growth. Most common reactive form is dissolved inorganic phosphorus (DIP) found as phosphate ([math]PO_4^{3-}[/math]). Phosphorus also occurs in the largely refractory form of dissolved organic matter (DOM) as dissolved organic phosphorus (DOP). Small amounts of phosphorus occur in the not directly usable form of particulate organic matter (POM).
  • Potassium ([math]K[/math])
  • Calcium ([math]Ca[/math])
  • Magnesium ([math]Mg[/math])
  • Sulfur ([math]S[/math])
  • Silicium ([math]Si[/math]), mainly as silicic acid [math]Si(OH)_4[/math] can be a limiting nutrient for diatoms

Nutrients needed in trace amounts

  • Iron ([math]Fe[/math]) can be a limiting nutrient
  • Boron ([math]B[/math])
  • Chlorine ([math]Cl[/math])
  • Manganese ([math]Mn[/math])
  • Zinc ([math]Zn[/math]) can be a limiting nutrient
  • Copper ([math]Cu[/math])
  • Nickel ([math]Ni[/math])
  • Molybdenum ([math]Mo[/math])

Eutrophication indicators

There are no widely applicable indicators of eutrophication due to the high variation in natural conditions and the interaction of multiple factors influencing eutrophication. Often Chlorophyll a ([math]Cl \, a[/math]) is used as indicator of eutrophication, as a proxy for phytoplankton biomass. However, the drawback of using of [math]Cl \, a[/math] as an indicator is that there can be no increase in [math]Cl \, a[/math] after nutrient concentrations have exceeded the threshold beyond which other factors (e.g. light, grazing) are limiting. Additionally, [math]Cl \, a[/math] measures only changes in the abundance of primary producers and cannot indicate any changes in community composition that may occur simultaneously (Jessen et al. 2015[6]).


Articles related to eutrophication

Eutrophication processes

Eutrophication impacts

Eutrophication monitoring

Eutrophication modelling

Eutrophication policy


References

  1. Nixon, S. W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41: 199–219
  2. HELCOM 2006[1]
  3. Andersen, J. H., Schlüter, L. and Ærtebjerg, G. 2006. Coastal eutrophication: recent developments in definitions and implications for monitoring strategies. J. Plankton Res 28(7): 621-628
  4. OSPAR, 2003. In: Strategies of the OSPAR commission for the protection of the marine environment of the north-east Atlantic (reference number: 2003e21)
  5. Howarth, R.W. 1988. Nutrient limitation of net primary production in marine ecosystems. Annual Rev. Ecol. Syst. 19: 89–110
  6. Jessen, C., Bednarz, V.N., Rix, L., Teichberg, M. and Wild, C. 2015. Marine Eutrophication. In: Armon, R., Hänninen, O. (eds) Environmental Indicators. Springer, Dordrecht