Nancy N. Rabalais
Nitrogen in Aquatic Ecosystems
Aquatic ecosystems respond variably to nutrient enrichment and altered nutrient ratios, along a continuum from
fresh water through estuarine, coastal, and marine systems. Although phosphorus is considered the limiting
nutrient for phytoplankton production in freshwater systems, the effects of atmospheric nitrogen and its contribution to acidification of fresh waters can be detrimental.
Within the estuarine to coastal continuum, multiple nutrient
limitations occur among nitrogen, phosphorus, and silicon
along the salinity gradient and by season, but nitrogen is
generally considered the primary limiting nutrient for phytoplankton biomass accumulation. There are well-established, but nonlinear, positive relationships among nitrogen
and phosphorus flux, phytoplankton primary production,
and fisheries yield. There are thresholds, however, where
the load of nutrients to estuarine, coastal and marine systems exceeds the capacity for assimilation of nutrientenhanced production, and water-quality degradation occurs. Impacts can include noxious and toxic algal blooms,
increased turbidity with a subsequent loss of submerged
aquatic vegetation, oxygen deficiency, disruption of ecosystem functioning, loss of habitat, loss of biodiversity,
shifts in food webs, and loss of harvestable fisheries.
INTRODUCTION
There is little doubt that reactive nitrogen (Nr) fixed by human
activities has increased substantially over the last one and a half
centuries and that anthropogenic nitrogen is accumulating in environmental reservoirs and altering many ecological processes
(Fig. 1) (1, 2). My goal in this paper that culminates from the
Second International Nitrogen Conference (Potomac, Maryland,
USA, October 2001) is to summarize the effects of increased inputs of nitrogen to aquatic ecosystems. It is impossible, however, to separate the nitrogen effects from other nutrient inputs
or other stressors, particularly at the community or ecosystem
level. Increased loads cannot be examined in isolation of other
nutrients essential to the growth of plants, namely phosphorus
and silicon (and micronutrients, such as iron). In combination
with increased flux of nitrogen to aquatic systems, similar
changes have occurred with phosphorus, and the loads of silicon have remained constant or decreased, often resulting in an
altered stoichiometric balance of nitrogen, phosphorus and silicon. Increased nutrients along with altered nutrient ratios cause
multiple and complex changes in aquatic ecosystems.
There are several excellent reviews of changes in nutrient
budgets on regional and global scales and the causative agents,
nutrient limitation of phytoplankton growth, and an expanding
body of literature on estuarine and coastal eutrophication and its
effects on living resources (e.g. 1, 3–14). Surprisingly, there remain several unresolved issues with regard to the importance of
increased nutrients—in particular, whether there is really an environmental problem, whether other environmental factors or
biological processes are more important than increased nutrients
in influencing ecosystem functioning and processes, what is the
level of nutrient enrichment above which there is degradation
of the environment and loss of living resources, what is the balance of necessary and excess nutrients for system productivity,
and what is the potential and time course for recovery of an eco102
system degraded by excess nutrients given that a suitable nutrient management program is put into place.
NUTRIENT SOURCES AND THEIR CHANGE
Human population growth and its associated activities have altered the landscape, hydrologic cycles, and the flux of nutrients
essential to plant growth at accelerating rates over the last several centuries (1, 2). Fossil-fuel consumption and food production in support of burgeoning human population growth have increased significantly the flux of nitrogen and phosphorus to
aquatic and terrestrial ecosystems with alterations of global cycles of those nutrients.
The inputs of reactive nitrogen (Nr) to the Earth’s ecosystem
increased by a factor of 20 since 1860 to the present production
of ~ 150 Tg N yr–1 (2). The forms of Nr that affect aquatic ecosystems include inorganic dissolved forms (nitrate, ammonium),
a variety of dissolved organic compounds (amino acids, urea,
and composite dissolved organic nitrogen (DON)), and
particulate nitrogen. Phytoplankton and higher plants utilize different forms of Nr preferentially, and the relative proportion, as
well as the load, of forms of Nr may differentially influence
phytoplankton growth, size structure, and community composition (e.g. 15, 16).
Phosphorus additions to the landscape enter via phosphoruscontaining fertilizers manufactured from mined phosphorus, animal manures, and waste products from animals supplemented
with phosphorus-enriched feed, and enter rivers and streams via
wastewater effluents and soil erosion. As phosphorus inputs to
the land exceed phosphorus outputs in farm products, phosphorus is accumulating in the soil with important implications for
increased runoff from the landscape to surface waters (17). Increased flux of phosphorus eroded from the landscape or carried in wastewater effluents to the world’s rivers increased the
global flux of phosphorus to the oceans almost threefold above
historic levels of ~ 8 million Tg P yr–1 to current loadings of
~ 22 Tg yr–1 (9, 17). Accumulation in landscapes of developed
countries is declining somewhat, but that of developing countries is increasing (17).
Rivers play a crucial role in the delivery of nutrients to the
ocean. These rivers terminate in the estuaries or in the nearshore
coastal ocean, where the effects of nitrogen enrichment are most
pervasive. In the sub-basins to the North Atlantic Ocean, specifically in the Baltic catchments, and in the watershed of the
Mississippi River, inputs of anthropogenic nitrogen via rivers far
exceed other sources of nitrogen input—atmospheric deposition,
coastal point sources, and nitrogen fixation (10, 18, 19). Phosphorus loads, likewise, come mostly from rivers (17, 19). Direct atmospheric deposition of nitrogen and phosphorus on estuaries and coastal waters may contribute as little as 1% to as
much as 30–40% of the total load (20). Clearly there are multiple pathways of increased inputs of nutrients to aquatic systems,
and the management of these nutrients must be multifaceted and
cross numerous boundaries (Fig. 1) (21–24).
Compared to increased runoff of nitrogen and phosphorus,
river concentration or loads or both of dissolved silicon have remained the same or decreased, so that the relative proportions
of silicon to nitrogen and silicon to phosphorus in river effluents have decreased over time as the nitrogen to phosphorus ra-
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Ambio Vol. 31 No. 2, March 2002
Atmosphere
NOx
Ozone
effects
Energy
production
Figure 1. The nitrogen cascade illustrating the
movement of nitrogen from one effect to
another as it cycles through environmental
reservoirs with emphasis (in red) on flows in
aquatic ecosystems or flows that lead to
aquatic ecosystems (modified from 1).
PM &
visibility
effects
NOx
Food
production
NHx
Stratospheric
effects
NH3
Crop
NH4
Forest & grasslands
Animal
Soil
Soil
People
(food, fiber)
Agroecosystem effects
Norg
Human activities
NO3
NO3
NO3
The
Nitrogen
Cascade
Greenhouse
effects
*
*
Groundwater
effects
*
NO3
Terrestrial ecosystems
NO3
NH4
*denitrification
Lakes, streamwater
& river effects
* NO
Coastal
effects
3
*
Ocean
effects
N20
Aquatic ecosystems
potential
tio increased (25, 26). The dissolved silicate:nitrate ratio is inversely correlated with various indices of landscape development
(e.g. population density, agricultural and economic intensity)
(26), and the percentage of world rivers approaching the Si:N
ratio of 1:1 (the Redfield ratio) will increase with further economic development. When the Si:N atomic ratio is near 1:1,
aquatic food webs leading from diatoms (which require silicon)
to fish may be compromised, as shown for the Mississippi Riverinfluenced continental shelf of the Gulf of Mexico (27) and for
the northwestern shelf of the Black Sea affected by a similarlyaltered Danube River (28–30). Shifts of dominant species in
phytoplankton communities as well as an increase in the frequency or size of harmful or noxious algal blooms may also occur (31, 32). Significant deviation from the Redfield ratio of
Si:N:P of 16:16:1 indicates a growth-limiting deficiency of any
single of these elements. Justić et al. (25) proposed that phytoplankton production became less dependent on any single
growth-limiting nutrient, more ‘balanced,’ and increasingly
higher for the same amount of nitrogen loading as the N:P, Si:P
and Si:N ratios simultaneously approached their respective
Redfield ratio.
PHYTOPLANKTON GROWTH LIMITATIONS
Nitrogen and phosphorus limit the growth of terrestrial plants,
phytoplankton, macroalgae and vascular plants in freshwater and
marine ecosystems, and silicon additionally limits the growth of
diatoms (3, 4, 8, 33, 34). Phosphorus is the primary limiting nutrient in most lakes and reservoirs, and phosphorus limitation in
freshwater environments has been demonstrated rigorously at
several hierarchical levels of system complexity (4). Nitrogen
is considered the primary limiting nutrient in marine waters (8,
35), but a similar rigorous demonstration of nitrogen limitation
across numerous marine waters has not been achieved as for
phosphorus in fresh waters (4). Most would agree that single
nutrient limitation of marine systems is an oversimplification.
Howarth (8) summarized that many estuarine and coastal marine ecosystems are probably limited by nitrogen, but phosphorus may limit production in some systems, and evidently during
certain seasons, and may also secondarily limit production in
combination with nitrogen. Over-enrichment with nitrogen and
phosphorus alters the ratios of nitrogen, phosphorus and silicon
to each other, such that silicon limitation may occur on a more
Ambio Vol. 31 No. 2, March 2002
frequent basis (27, 34, 36). Conley (37) reviewed nutrient limitation in estuarine systems and concluded that many estuarine
systems display phosphorus limitation in the spring and switch
to nitrogen limitation in the summer with some estuaries displaying dissolved silicate limitation of the spring diatom bloom.
Similar spatial and seasonal, or longer-term, variability in nutrient limitation are apparent in the influence of the Mississippi
and Danube Rivers (38, 39). There is a need to distinguish between the processes of biomass limitation and growth-rate limitation. If the concern with increased nutrient loads is eutrophication, then biomass accumulation is the important issue, and
accumulation of biomass in most coastal marine systems is nitrogen limited, as shown for Chesapeake Bay (40, 41) and over
the broad region of the northern Gulf of Mexico influenced by
the Mississippi River and subject to hypoxia (42).
Data for oligotrophic, oceanic waters indicate that they are also
likely limited by nitrogen preferentially to phosphorus over short
time scales, but that both may limit. Another essential element,
iron, supplied mainly from atmospheric dust, is also usually in
short supply. Fixed nitrogen is a limiting nutrient in much of the
ocean, and until recently, the large, nitrogen-fixing cyanobacteria
Trichodesmium were considered the primary source of ‘new’ nitrogen in the open ocean. New evidence is that single-celled
cyanobacteria (3–10 µm, the nanoplankton) actively express the
nitrogenase gene that allows nitrogen fixation to a biologically
useful form and are abundant enough to play a major role in the
oceanic nitrogen cycle (43), but their growth may be constrained
by limited supply of the essential elements, phosphorus and iron.
There are large differences, however, in the processes driving
nutrient enrichment of coastal waters from those in the open
ocean far removed from the direct effects of anthropogenic nutrient enrichment.
NUTRIENT-ENHANCED PRODUCTIVITY
Significant positive relationships exist between nutrient-loading
rates and algal production and biomass (13, 44, 45), but nonlinearly because of the large differences among estuaries in the
rates or pathways through which external nutrients are converted
into algal biomass (see Figs 2 and 3).
Boynton and Kemp (48) pursued the nutrient-algal biomass
and production relationships in Chesapeake Bay further in a linear regression analysis of river flow (strongly correlated with
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103
Phytoplankton production (g C m–2 yr–1)
Primary production, g C m–2 yr–1
10 000
1000
100
Annual N loading (mol N m–2 yr–1)
10
0.1
1
10
100
DIN input, mol m–2 yr–1
Mean primary
production (g C m–2 d–1)
Figure 2. Left panel: the
relationship between the
input of dissolved
inorganic nitrogen (DIN)
per unit area and primary
production in a variety of
marine systems (45, with
kind permission of Kluwer
Academic Publishers).
The open circles are from
mesocosm tanks (13 m3)
at the Marine Ecosystems
Research Laboratory
(MERL) at the University
of Rhode Island. Natural
systems are solid circles.
Right panel: the relationship between annual
phytoplankton production
vs nitrogen loading of
different coastal areas
(from 46 as modified in
13). Note that data are
presented logarithmically
(left panel) or not (right
panel).
5
5
5
4
4
4
3
3
3
2
2
2
1
1
1
0
0
0
100
200
300
400
NO3 + NO2 flux (106 mol d–1)
0
100
200
NO3 + NO2 (µM)
300
0
1
2
3
4
Orthophosphate (µM)
5
Figure 3. Relationship between mean primary production for the combined central and eastern regions of the
Mississippi River bight and riverborne nitrate and nitrite flux, nitrate and nitrite concentration at Venice, and
orthophosphate concentrations at Belle Chase (47). Historical primary production data ca. 1950s are shown for
comparison in panels a and b (open circles). An outlier for March 1991 is indicated by an arrow; this lower production
was constrained by available light. (Publ. with kind permission of Inter-Research Science Publisher).
nutrient flux) and phytoplankton production and biomass, spring
deposition of chlorophyll a, and seasonal declines in deep-water dissolved oxygen. With appropriate combinations of river
flow (average of current and previous year, flow during winter
and spring before deposition of chlorophyll), they demonstrated
strong relationships of river flow with primary production and
the fate of that production. They further demonstrated a strong
relationship between the deposition of the production in the form
of sedimented chlorophyll a and the seasonal decline of deepwater dissolved oxygen. While these relationships do not negate
the importance of water-column stratification and other physical processes, they do clearly link quantitatively nutrient flux
with eventual degradation of water quality in the form of chronic,
seasonal oxygen deficiency. These same relationships held in an
intra-site comparison within Chesapeake Bay, where overall
there were strong and linear relationships of primary production,
benthic-pelagic coupling, and nutrient recycling to both freshwater load and nutrient-loading rates.
Similar relationships have been identified for the Mississippi
River-influenced area of the northern Gulf of Mexico continental shelf where severe seasonal hypoxia develops most summers
(42). High biological productivity in the immediate and extended
plume of the Mississippi River is mediated by high nutrient inputs and regeneration, favorable light conditions, and suitable
temperature, salinity, and mixing rates (49, 50). Lohrenz et al.
(47) demonstrated that primary production in shelf waters near
the delta and to some distance from it was significantly correlated with nitrate and nitrite concentrations and fluxes over the
period 1988 to 1994 (Fig. 3). Light limitation was likely an important factor during winter months, but a positive correlation
104
was demonstrated between river inputs of nitrate and nitrite for
other times of the year. Even stronger correlations were observed
between the concentration of orthophosphate and primary production, but these were not significant (smaller sample size).
There was also a high degree of coherence between Mississippi
River nitrate flux and net production at a 20-m water depth station in the core of the hypoxic zone 90 km down-plume from
the Mississippi River influence for 1985–1992 (51).
Data from 36 marine systems show a positive relationship between fisheries yield and primary production (52) (Fig. 4). On
the other hand, a meta-analysis of 47 marine food webs including open systems (53) indicated that in open systems the availability of nitrogen and the primary production rate were strongly
correlated to the accumulation of phytoplankton but not to higher
trophic levels (summarized in 54). Micheli’s analysis (53) demonstrated a weak coupling between phytoplankton, mesoplankton
and zooplankton for closed and manipulated systems.
Grimes (55) pointed out that 70–80% of the Gulf of Mexico
fishery landings comes from the water surrounding the Mississippi River delta, a river that has witnessed a tripling of nitrate
loads in the last half of the 20th century. While the mechanisms
for the apparent enhancement of marine fisheries are not clear,
he proposed that enhanced recruitment was the most likely process. Enhanced recruitment, i.e., larval production, feeding,
growth and survival, are likely facilitated by both the physical
characteristics of the river plume (areas of convergence, stratification, and transport and retention of fish larvae) and biological dynamics that favor processes that regulate recruitment. Similar enhancement of fisheries production in Mediterranean waters is found in areas under the influence of river effluents (56).
© Royal Swedish Academy of Sciences 2002
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Ambio Vol. 31 No. 2, March 2002
1000
10
ESTUARIES
(
macrophytes important)
SHELF
UPWELLING
OTHER MARINE
AFRICAN LAKES (Melack 1976)
100
g C m–2 yr–1
1%
Fisheries, kg ha–1 yr–1
1.0
10
0.1
36 MARINE
SYSTEMS
r–1 = 0.84
OGLESBY (1977)
r–2 . 0.74
15 LAKES > 10 km2
0
0
1000
100
Primary production, g C m–2 yr–1
Figure 4. Relationship between fisheries yield per unit area and primary
production per unit area across a spectrum of aquatic ecosystems (52).
The r2 for regressions for marine systems and freshwater lakes are
superimposed. (Publ. with kind permission of the American Association
of Limnology and Oceanography).
There are thresholds, however, where the load of nutrients to a marine system exceeds the capacity for assimilation, and water-quality degradation occurs with detrimental effects on components of the ecosystem and on
ecosystem functioning. Caddy (57) illustrated how an increase in nutrient input results in a continuum of fisheries yield with an increase to a maximal point as nutrient
load increases, then a decline in various compartments of
the fishery as seasonal hypoxia and permanent anoxia (no
oxygen) become features of semi-enclosed seas (Fig. 5).
Documenting loss of fisheries related to the secondary effects of eutrophication, such as the loss of seabed vegetation and extensive bottom-water oxygen depletion is
complicated by poor fisheries data, inadequate economic
indicators, increase in overharvesting that occurred at the
time that habitat degradation progressed, natural variability of fish populations, shifts in harvestable populations,
and climatic variability (14, 56, 58, 59). Eutrophication
of surface waters accompanied by oxygen deficient bottom waters can lead to a shift in dominance of fish stocks
from demersals to pelagics. In the Baltic Sea and Kattegatt
where eutrophication-related ecological changes occurred
mainly after World War II (60), changes in fish stocks
have been both positive, due to increased food supply (e.g.
pike perch in Baltic archipelagos) and negative (e.g. oxygen deficiency reducing Baltic cod recruitment and eventual harvest). Similar shifts are hinted at with limited data
on the Mississippi River-influenced shelf with the increase
in selected pelagic species in bycatch from shrimp trawls
and a decrease in certain demersal species (61). In the case
of commercial fisheries in the Black Sea, it is difficult to
discern the impact of eutrophication through the loss of
macroalgal habitat and oxygen deficiency or a shift in the
system from dominance by benthic production to pelagic
production as eutrophication advanced, amid the possibility of overfishing. After the mid-1970s, benthic fish
populations (e.g. turbot) collapsed, and pelagic fish
Figure 5. The generalized
relationship of
production and fishery
yield as nutrient loading
increases with varying
effects of eutrophication
expressed as seasonal
and permanent bottomwater anoxia; a spectrum
of enclosed seas
(modified from 13, with
kind permission of InterResearch Science
Publisher).
Ambio Vol. 31 No. 2, March 2002
© Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
105
populations (small pelagic fish, such as anchovy and sprat)
started to increase. The commercial fishery diversity declined
from 25 fished species to about 5 in 20 years (1960s to 1980s),
while anchovy stocks and fisheries increased rapidly (39). The
point on the continuum of increasing nutrients versus fishery
yields remains vague as to where benefits are subsumed by environmental problems that lead to decreased landings or reduced
quality of production and biomass.
the trophic structure of surface waters. Besides direct mortality
to acid-sensitive fish from acidic waters, inorganic monomeric
Al is directly toxic to fish and increases as the pH decreases in
aquatic ecosystems. The effects of Al toxicity are ameliorated
somewhat where Ca2+ is higher in lakes. Surface-water acidification enhances mercury accumulation in fish. Acidification of
surface waters results in a decrease in the survival, size, and density of fish and in the loss of fish and other aquatic biota from
lakes and streams.
NUTRIENT ENRICHMENT ALONG THE FRESHWATER TO MARINE CONTINUUM
The effects of nitrogen enrichment in the environment are numerous, including both beneficial and detrimental, as the various forms of biologically available nitrogen cascade through the
various reservoirs within a landscape and ultimately end up in
ocean sediments or are returned to the atmosphere as nonreactive
dinitrogen gas (Fig. 1) (1). Primary producers are the first component of the ecosystem to respond to increased nutrient loads
by increased production. Eutrophication, as defined by Nixon (7),
is the increased accumulation of organic matter, usually as a result of increased nitrogen and phosphorus inputs, but could result from the supply of excessive decomposable organic carbon
as well.
Where excess carbon is produced and accumulates, secondary effects of eutrophication often occur such as noxious algal
blooms (including some toxic ones), decreased water clarity, and
low dissolved oxygen. The ultimate symptom is a loss or degradation of habitat with consequences to marine biodiversity and
changes in ecosystem structure and function, such as cycling of
elements and processing of pollutants. There are many examples of localized or temporary loss of biodiversity, shifts in community structure in both pelagic and benthic systems, and degraded habitats, such as coral reefs, seagrass beds, and productive continental shelves with important commercial fisheries that
become unsuitable for the usual inhabitants. Over the last two
decades it has become increasingly apparent that the effects of
eutrophication are not minor and localized, but have large-scale
implications and are spreading rapidly (7, 62, 63).
Estuarine and Coastal Systems
Eventually, there is a large flux of a variety of nitrogenous and
phosphorus forms off the landscape and into streams and rivers
and from the atmosphere that are delivered to estuaries and the
coastal ocean. Primary producers are the first component of the
ecosystem to respond to increased nutrient loads by increased
production. This includes a suite of plants, including phytoplankton, benthic macrophytes such as sea grasses, filamentous
algae, and macroalgae. One of the secondary effects of increased
phytoplankton production is an increase in turbidity and a decrease in the penetration of light through the water column. Welldocumented examples of decline in Secchi disk depth with increases in nutrient loads to coastal systems exist for the northern Adriatic Sea, the Baltic Sea, and the northern Gulf of Mexico
(38, 60, 67) (Fig. 6).
Increased turbidity from excess phytoplankton growth in the
upper water column can affect the amount of light reaching submerged aquatic vegetation, which in turn limits their growth, and
ends in the demise of these structurally complex habitats and the
functions they serve as refuge, feeding and nursery areas for fish
and invertebrates. Excess nutrients can also stimulate the growth
of epiphytic algae on the blades of submerged aquatic vegetation or increase the incidence of drifting macroalgae (68). Typical of nutrient-enriched temperate and tropical regions are ‘nuisance’ macroalgae, typically the filamentous or sheet-like forms
(Ulva, Cladophora, Chaetomorpha, Gracilaria) that accumulate
in extensive, thick unattached mats over seagrasses or the sediment surface. Increased turbidity from increased phytoplankton
biomass also decreases the light penetration within the euphotic
zone of estuarine and coastal waterbodies, which results in a decrease of light availability for photosynthetic, oxygen-producing microphytobenthos.
Johansson and Lewis (69) described the effects of nutrient
loading on water quality and seagrass communities in Tampa
Bay, Florida. In the 1950s, Tampa Bay was ‘grossly polluted’
with organic and nutrient enrichment from cannery wastes,
poorly treated municipal sewage, phosphate mines, and other industrial sources. Obvious signs of eutrophication in Tampa Bay
106
Figure 6. The change in the Secchi disk depth on the Louisiana shelf
west of the Mississippi River delta for the period indicated (38). The
data are restricted to stations with surface-water salinity between 20
and 25 psu and depths between 10 and 100 m. The slope of the
regression line is significant at the 8% level of significance.
The error bars are ± s.e.
6
Average Secchi disk (m)
Freshwater Systems
The nutrient considered to be the critical limiting nutrient and
the one of concern for eutrophication of freshwater systems is
phosphorus, but evidence points to combinations of phosphorus
and nitrogen as limiting for both algae and vascular plants in a
variety of freshwater systems, including lakes, reservoirs, and
streams (64). The cases for the singular limitation by nitrogen
in freshwater systems are much less common. Lakes that become
eutrophied, primarily because of an excess of phosphorus, are
typically characterized by a shift towards the dominance of
phytoplankton by cyanobacteria, including noxious forms several of which are toxin producers. On terrestrial landscapes and
the freshwater systems into which they drain, increased inputs
of nitrogen manifest in ways other than eutrophication. Excess
atmospheric deposition of nitrogen to temperate forests can lead
to increased productivity but loss of biodiversity; the effects on
tropical systems are less well known (65). Once nitrogen is transformed through microbial processes in soils to biologically available nitrogen in ground and surface waters, there are a number
of effects beginning with groundwater contamination and surface-water acidification.
Freshwater systems that are poorly buffered by surrounding
soils can be acidified by increased deposition of nitrate and ammonium. The continuing acidification of Europe, northeastern
North America and parts of Asia is now increasingly a nitrogen-pollution rather than a sulfur-pollution problem (66). The
acidic deposition has resulted in the acidification of soil waters,
shallow groundwater, streams, and lakes with marked effects on
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1980
© Royal Swedish Academy of Sciences 2002
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Ambio Vol. 31 No. 2, March 2002
Harmful Algal Blooms
Excessive phytoplankton growth in response to nutrient increases
or shifts in nutrient ratios or both may result in a bloom of a
single species that has some negative impact. These events are
typically called harmful algal blooms, or HABs, and variously
encompass red tides, brown tides, and toxic and noxious blooms.
Toxic forms may directly affect a variety of life forms, such as
macroalgae, invertebrates, and vertebrates, including humans,
Ambio Vol. 31 No. 2, March 2002
Figure 7. The qualitative changes in phytoplankton and macroalgal
communities with increasing eutrophication from left to right through
stages I–IV as described in text (modified from 72, with kind permission
of Kluwer Academic Publishers).
A
Seasonal fast growing
nutrient opportunists
epiphytes
Relative dominance
of primary producers
Free floating
macroalgae
Perennial benthic
macrophytes
Phytoplankton
B
Light
penetration
Increasing
were high turbidity, anoxia of bottom waters, large amounts of
drift macroalgae in the shallows, and loss of most of the submerged sea grasses in Hillsborough Bay segment by the 1960s.
By 1982 about 20% of the originally estimated coverage of
Tampa Bay seagrasses remained (see section on Recovery). Prolonged and persistent brown tides (Aureoumbra lagunensis in
the Laguna Madre, Texas and Aureococcus anophagefferens in
estuaries from Narragansett Bay, Rhode Island, to Barnegat Bay,
New Jersey) detrimentally affected seagrass beds and suspension-feeding bivalves, including bay scallops (70, 71).
Where macroalgae are the dominant component of the marine
ecosystem, there is a fairly predictable series of shifts in species as eutrophication increases (72) (Fig. 7). i) In uneutrophied
marine or brackish shallow coastal waters, the dominant producers are usually perennial benthic macrophytes, such as seagrasses
and other phanerogams on soft bottoms, or long-lived seaweeds
on hard substrata. ii) In the stages of slight to medium eutrophication, increased nutrient loading favors the growth of bloomforming phytoplankton and fast-growing, short-lived epiphytic
macroalgae over slow-growing, long-lived macrophytes. Phanerogams and perennial macroalgal communities gradually decline along with changes in the structure (species composition,
coverage, or depth distribution limits) and their function (production and reproduction). iii) With increased nutrient loads towards hypereutrophic conditions, free-floating macroalgae,
in particular ‘green tide’ forming taxa such as Ulva and
Enteromorpha alternate with dense phytoplankton blooms in
dominance and replace the perennial and slow-growing benthic
macrophytes until their extinction. iv) Under hypereutrophic conditions, phytoplankton constitute the dominant primary producers and benthic macrophytes disappear completely. This sequence of events is not gradual but is stepwise with sudden shifts.
Schramm (72) provided numerous examples of this sequence
throughout European waters, with some variability among sites.
Other factors besides nutrients, such as changes in light regime,
hydrological conditions, and grazing communities, influence or
determine the varying responses of benthic macroalgae to increased nutrient levels. Similarly, data from joint nutrient enrichment and grazer experiments in seagrass beds indicate complex
interactions among nutrients, light conditions, structural changes,
and grazing pressure (73).
Clear water and rocky shores with dense growth of the brown
seaweed bladderwrack (Fucus vesiculosus) that provided spawning and nursery grounds for many fish (74) characterized the
Baltic Sea in the 1940s. Today, filamentous green and brown
algae shade the bladderwrack and may even totally replace it.
The cause of these changes is increased plankton blooms and
organic particle production that reduced light penetration by 3
m compared to the first half of the century (75). Because of the
reduced water clarity, the bladderwrack, the ‘kelp rainforest’ of
the Baltic, cannot grow at the same depth. The lower growth
limit has been moved up by about 3 m since the 1940s, and it
does not now grow as densely as before (76). The functions of
the bladderwrack beds (habitat for refuge from predators, source
of prey, and location as spawning and nursery grounds) are compromised and no longer support many species previously found
there. A similar loss of massive beds of red macroalgae occurred
on the northwestern shelf of the Black Sea with concomitant loss
of fisheries stocks that were supported by that habitat (39).
Relative levels of chemical
and physical parameters
Nutrient
level
Stable
substrate
Resuspension
and indirectly cause impacts through the consumption of toxins
accumulated in fish and shellfish. Less obvious impacts are reduced grazing, increased flux of organic matter leading to hypoxia, and changes in trophic dynamics.
There has been some debate as to whether the frequency of
harmful algal blooms has increased, but several researchers suggest a clear global expansion (77). Temporal trajectories of increased occurrence of HABs with increased nutrient loads are
repeatable worldwide, but other factors, such as increased awareness and reporting, changes in freshwater inflow and circulation
patterns, and worldwide transport via ship ballast water, may also
be important. Compelling evidence points to a linkage between
nutrient loading and the often-cited increased frequency of harmful algal blooms in the Seto Inland Sea, Japan (78). Red-tide outbreak frequency increased by an order of magnitude (from 40
to more than 300 annually) between 1965 and 1975 as nutrient
loading increased. Bloom frequency was reduced by half in subsequent years following a 50% reduction in nutrient loading in
1972. The frequency of red tides peaked in 1975 and has been
declining ever since. Other lines of evidence link cultural eutrophication to several HAB species (79). Harmful algal blooms,
in general, however, cannot always be linked to nutrient overenrichment.
Nutrient enrichment (both nitrogen and phosphorus) of fresh
and brackish environs leads to increasing blooms of cyanobacteria that result in hypoxia, toxicity to aquatic organisms, foul
odors, tainted fish products, and fish kills (80). The bloom of
toxin-producing colonial cyanobacteria in oligohaline Lake
Pontchartrain in 1997 was clearly related to the diversion of nitrogen-enriched water from the Mississippi River (81). Pfiesteria
piscicida, a dinoflagellate responsible for massive fish kills in
Pamlico-Albemarle Sound, North Carolina and serious neurological human health risks, is associated with high organic loading from sewage or animal wastes (hog or chicken) (82, 83). The
toxin-producing forms of the diatom Pseudo-nitzschia occur in
the northern Gulf of Mexico (84) often in bloom proportions,
the seasonal abundance correlates with high dissolved inorganic
nitrogen flux from the Mississippi River (85), and the abundance
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107
appears to have increased dramatically since the 1950s coincident with human-related increases in riverine nitrogen flux (86,
87). Thus, there is evidence for the linkage of nutrient overenrichment to some toxic forms that kill or debilitate higher organisms and the formation of nontoxic but noxious blooms that
lead to other habitat impairments.
Oxygen Depletion and Associated Processes
A central concept in eutrophication is that nutrient enrichment
can, in some estuarine and coastal systems, stimulate biomass
accumulation of phytoplankton, enhance flux of that fixed carbon to bottom waters, and lead to the development of hypoxia
or anoxia (13). Dead and senescent algae and zooplankton fecal
pellets contribute significant amounts of organic detritus to the
lower water column and seabed. Aerobic bacteria consume oxygen during the decay of the carbon and deplete the oxygen in
the lower water column at a faster rate than the diffusion of oxygen from surface waters to bottom waters. Hypoxia will persist
as long as oxygen consumption rates exceed those of resupply.
Oxygen depletion occurs more frequently in estuaries or coastal
areas with longer water residence times, higher nutrient loads,
and stratified water columns (12).
In a review of 47 known anthropogenic hypoxic zones, Diaz
and Rosenberg (63) noted that no other environmental variable
of such ecological importance to estuarine and coastal marine
ecosystems around the world has changed so drastically, in such
a short period of time, as dissolved oxygen. Most hypoxic zones
are annual summertime events, and some instances may result
from natural conditions. For those reviewed by Diaz and Rosenberg (63), however, there was a consistent trend of increasing
severity (either duration, intensity, or size) where hypoxia occurred historically, or hypoxia existed presently when it did not
occur before. While hypoxic environments have existed through
geologic time and are common features of the deep ocean or adjacent to areas of upwelling, their occurrence in estuarine and
coastal areas is increasing and the trend is consistent with the
increase in human activities that result in nutrient overenrichment. The coastal areas of the Baltic Sea, northern Gulf of
Mexico, and northwestern shelf of the Black Sea are the largest
such coastal hypoxic zones in the world, reaching 84␣ 000 km2,
21␣ 000 km2, and 40␣ 000 km2 (until recently), respectively (39,
62, 88) (see Figure 8 for representative Gulf of Mexico bottomwater hypoxia distribution). Hypoxia existed on the northwestern Black Sea shelf historically, but anoxic events became more
frequent and widespread in the 1970s and 1980s (28, 29, 39),
reaching over areas of the seafloor up to 40␣ 000 km2 in depths
of 8 to 40 m. There is also evidence that the suboxic zone of
the open Black Sea enlarged towards the surface by about 10 m
since 1970. Following substantially decreased input of nutrients
to the Black Sea beginning in the 1990s, the size of the hypoxic
area there became negligible or nonexistent by the end of the
century (39) (see section on Recovery).
The obvious effects of hypoxia/anoxia are displacement of
pelagic organisms and selective loss of demersal and benthic
organisms (14). These impacts may be aperiodic so that recovery occurs, recurring on a seasonal basis, or permanent so that
long-term ecosystem structure and function shifts. As the oxygen concentration falls from saturated or optimal levels towards
depletion, a variety of behavioral and physiological impairments affect the animals that reside in the lower water column
or in the sediments or attached to hard substrates. Mobile animals, such as shrimp, fish, and some crabs, flee waters where
the oxygen concentration falls below 3 to 2 mg L–1. As dissolved oxygen concentrations continue to fall, less mobile organisms become stressed and move up out of the sediments,
attempt to leave the seabed, and often die. As oxygen levels
fall from 0.5 mg L–1 towards 0 mg L–1, there is a fairly linear
decrease in benthic infaunal diversity, abundance, and biomass.
Losses of entire higher taxa are features of the depauperate
benthic fauna in the severely stressed seasonal hypoxic/anoxic
zone of the Louisiana inner shelf in the northern Gulf of Mexico
(14). Larger, longer-lived burrowing infauna are replaced by
short-lived, smaller surface deposit-feeding polychaetes, and
certain typical marine invertebrates are absent from the fauna,
for example, pericaridean crustaceans, bivalves, gastropods, and
ophiuroids. The hypoxia-affected fauna in Chesapeake Bay is
characterized by a lower proportion of deeper-burrowing equilibrium species such as long-lived bivalves and a greater dominance of short-lived surface-dwelling forms (89). Long-term
trends for the Skagerrak coast of western Sweden in semi-enclosed fjordic areas experiencing increased oxygen stress (90)
showed declines in the total abundance and biomass of macroinfauna, abundance and biomass of mollusks, and abundance
of suspension feeders and carnivores. These changes in benthic
communities result in an impoverished diet for bottom-feeding fish and crustaceans and contribute, along with low dissolved oxygen, to altered sediment biogeochemical cycles.
As aerobic bacteria decompose the increased organic matter
settling onto the seabed and the dissolved oxygen concentration overlying the sediments approaches anoxia, numerous biological and geochemical shifts occur in the benthic community,
many with negative feedback into the cycle of eutrophication
and declining oxygen levels. With increasing eutrophication,
concentrations of organic carbon and nitrogen, microbial biomass, microbial decomposition potential of substrates, and community oxygen consumption increase, but not in simple linear
relationships (91). The redox potential discontinuity layer migrates upward to the sediment-water interface, sulfate respiration replaces oxygen respiration, hydrogen sulfide is generated
from the sediments, and oxygen penetrates less deeply into
the sediments as the bioturbation potential of the macroinfauna decreases during their demise due to sulfide toxicity
or lack of sufficient oxygen. The sediments become less cohesive, more susceptible to resuspension, and contribute to tur-
Figure 8. Distribution of
bottom-water dissolved
oxygen values less than 2
mg L–1 during a shelfwide
assessment cruise in late
July 2001; the area is
20 700 km2 (88).
108
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Ambio Vol. 31 No. 2, March 2002
Figure 9. Interactions of nitrogen and
phosphorus cycling in oxic vs anoxic
sediments (modified from 105, with kind
permission from the Dalhem Workshop
Report “Science and Integrated Coastal
Management”, Dalhem University Press).
Overlaying water
Organic matter
Organic matter
Lost from
system
Recycled
bidity of the overlying water, which in turn reduces the potential for growth of the photosynthetic microphytobenthic community and generation of oxygen into the lower water column. Some
shifts in the benthic microbial community are visible at the sediment-water interface. Typical black spots from iron sulfide precipitated from intense microbial degradation of organic matter,
lacey white colonies and denser, yellowish colonies of sulfuroxidizing bacteria (Beggiatoa spp. and Thiovulum sp.), and reddish to violet carpets of sulfur-purple bacteria can be observed
as oxygen levels decline in the Wadden Sea (North Sea), in shallow water areas of the Baltic, on the Louisiana continental shelf,
and many areas of the world’s ocean where the oxygen minimum zone intersects the seabed (14).
Several microbially-mediated processes in sediments at the
surface of the seabed are altered as overlying waters become anoxic, often with negative feedback loops to continued degradation of water quality (92; Fig. 9). The nitrification/denitrification
cycle of estuarine and continental shelf sediments, which returns
N2 to the atmosphere is an ameliorating mechanism to excess
Nr, but the nitrification portion of this cycle is disrupted by the
lowered availability of oxygen in overlying waters. With the shift
in redox potential in the sediments with decreasing oxygen concentration, there is an increase in the flux of inorganic nutrients,
ammonium and particularly phosphate, into the overlying water. These inorganic nutrients become available to fuel further
phytoplankton production in the overlying water. The degree to
which these nutrients diffuse upward through the water column
and across strong pycnoclines is not known.
Coral Reefs
Many human activities affect the ‘health’ of coral reefs worldwide (93). Increased urbanization, deforestation, and expanded
agricultural activities contribute sediment and nutrient loads to
coastal waters. Sediments can directly smother corals. Untreated
or partially-treated sewage is discharged or permeates into waters surrounding many coral reefs. Direct destruction in construction projects, removal of specimens, and overfishing have direct
or indirect effects on reefs. Increasing water temperature is the
primary factor in coral bleaching and subsequent diseases. Coral
diseases are a serious cause of coral decline and may be aggravated by excess nutrients. The interaction of these many human
activities and their resultant nutrient, sediment and pollutant
loads make it difficult to understand how increasing nutrient
loads alone impact coral reefs, but increasing nutrients are conAmbio Vol. 31 No. 2, March 2002
sidered responsible for deteriorating water quality and loss of
reefs in Kaneohe Bay, Hawaii, parts of the Indian Ocean and
the Florida reef tract (e.g. 94–96).
The overgrowth of the macroalga Disctyosphaeria cavernosa
on reef slopes and outer reef flats in Kaneohe Bay is generally
attributed to nutrient enrichment resulting from sewage discharge
in the 1960s and 1970s (94). Twenty years after sewage diversion, D. cavernosa cover on reef slopes decreased substantially
in southern Kaneohe Bay, the site of most of the historical sewage discharge, but has changed less in other regions, remaining
high in the central bay and low in the north bay. The remnants
of this macroalga are explained by reduced grazing intensity on
D. cavernosa in preference for several introduced macroalgae
on reef flats (97). The complicating factors of nonindigenous
species and shifted trophic interactions obscured clear lines of
evidence between nutrient enrichment and coral reef decline.
The effects of nutrients on coral reef organisms have been
demonstrated in the laboratory, and there are many examples of
coincidental reef decline with nutrient enrichment in surrounding waters. The intensive ENCORE experiment (Enrichment of
Nutrients on a Coral Reef Experiment) on 12 pristine coral atolls of the Great Barrier Reef (98) demonstrated that reef organisms and processes were impacted by elevated nutrients, that
impacts included positive responses, that impacts were dependent on dose level, whether nitrogen and/or phosphorus were elevated, and that they were often species-specific. The results of
these experiments, however, are viewed as equivocal by at least
one author (99), who further stated that a causal link between
nutrification and coral reef decline is not clear and remains controversial. The discourse on this controversy promises to continue for some time.
Nutrient effects on coral reefs are likely to be more evident
in bays and confined water-bodies rather than well-flushed oceanic reefs. Nutrients are probably less important than other factors in causing reef declines in most locations, but they may be
aggravating the negative effects of other factors in ways that are
difficult to assess.
Oceanic systems
In more open ocean, pelagic systems removed from riverine influences, atmospheric and advective (upwelling/deep mixing)
nutrient inputs may be the key sources of ‘new’ nutrients supporting primary production. Both wet and dry atmospheric deposition contain various biologically reactive nitrogen forms, and
© Royal Swedish Academy of Sciences 2002
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109
atmospheric deposition of continental dust is the primary source
of new iron to the oceans. In a review of atmospherically-derived nitrogen as ‘new’ nitrogen inputs in diverse estuarine,
coastal and open-ocean waters, Paerl et al. (20) compiled estimated percentages for the Baltic Sea proper (> 25%), western
Baltic Sea Kiel Bight (60%), western Mediterranean Sea (10–
60%), North Pacific Ocean surface waters (40–70%), and Sargasso Sea surface waters (25%) and indicated that atmospheric
source nitrogen can be a major percentage of ‘new’ nitrogen
available to phytoplankton in oceanic waters. Bioassay experiments on offshore and Gulf Stream waters off North Carolina
and Sargasso Sea waters with a series of nitrogen forms, phosphate, micronutrients, and natural and simulated rainfall indicated
a broad sensitivity of these waters to nitrogen additions, which
in the case of nitrate were enhanced by Fe-EDTA (100). The high
level of stimulation of primary production attributable to natural rain may be due to the supply of both dissolved inorganic
nitrogen and co-limiting nutrients (e.g. Fe). Two recent studies
point to the importance of aeolian iron fluxes and nitrogen fixation by the nitrogen-fixing cyanobacteria Trichodesmium. Berman-Frank et al. (101) suggest that iron fluxes will
become more limiting for nitrogen fixation by Trichodesmium
in the coming century, based on present trends in the hydrological cycle. Lenes et al. (102) note the stimulatory effect of summer delivery of iron in the form of Saharan dust to the
oligotrophic waters of the eastern Gulf of Mexico in stimulating Trichodesmium blooms there over the last 50 years, and further point out the potential connection between regenerated nitrogen forms from the blooms and the stimulation of blooms of
the toxic dinoflagellate Gymnodinium breve (= Karenia brevis).
losses from land to sea following nutrient reductions actually
achieved or planned (104). On the time scale of a few years,
changes in the anthropogenic impact on water quality may easily be overshadowed by natural fluctuations in climate. These
facts are relevant to management strategies to mitigate nutrient
loads to estuaries and coastal waters, and the perceived projection for ‘recovery’.
Public and private funds have been expended within the
Chesapeake Bay watershed to reduce the controllable sources of
nitrogen and phosphorus entering the bay by 40% by the year
2000 (105). Efforts targeted both point sources, treated sewage
discharges, and nonpoint sources, especially those from agriculture, or to trap the nutrients in the watershed by wetland and
riparian-zone restoration. Assessing whether the reduction targets were reached was difficult, but it appears that the goal was
nearly met for phosphorus, but nitrogen loadings, although reduced, did not achieve the goal. Similarly, Grimvall et al. (104)
reported that there was a remarkable lack of response in eastern
European river nutrient loads in response to the dramatic decrease in the use of commercial fertilizers that started in the late
1980s. In western Europe, while studies of decreased phosphorus emissions have shown that riverine phosphorus loads can be
rapidly reduced from high to moderate levels, a further reduction, if achieved at all, may take decades.
Within estuaries and coastal systems, decrease in external nutrient loads does not produce an immediate shift in the eutrophic
condition of the system, in part because of the continued
remineralization of labile carbon and releases of regenerated nutrients. Boynton and Kemp (48) suggested a ‘nutrient memory’
over time scales of a year rather than seasonal periods as suggested by Chesapeake Bay water residence times. Assessing the
‘recovery’ of Chesapeake Bay in response to the nutrient load
reductions achieved so far is complicated by numerous factors,
but one indicator that could be attributed to reduced nutrients is
a return of seagrasses to some regions, although the present coverage is only a small portion of the habitat occupied in the 1950s
(105). Justić et al. (51) suggested that at least a year of continued carbon respiration following high deposition of carbon in a
flood year contributed to oxygen demand on the Louisiana continental shelf in the subsequent summer.
The severe degradation of water quality in Tampa Bay and
loss of valuable habitat, particularly seagrass beds, was followed
Thousands of km2 of
hypoxia (km2 . 103)
RECOVERY AND NUTRIENT MANAGEMENT
Howarth (8) noted that, given our understanding of nutrient limitation and knowledge of increasing inputs of nutrients to coastal
systems, to control eutrophication in these systems requires nitrogen controls, but that phosphorus controls also make sense.
Conley (37) expanded upon this generalization by stating that
potential reductions in phosphorus may help oxygen depletion
especially in deep estuaries and reduce fast-growing macrophytes
such as Ulva sp., although phosphorus reductions probably will
have little effect on summer chlorophyll concentrations. Reductions in nitrogen loading
should reduce summer chlorophyll concentraFigure 10. The relationship of nitrogen loads to the northwestern shelf of the Black Sea vs
the size of the bottom-water hypoxic zone for the periods indicated (39, with kind
tions and improve the conditions for subpermission of Dalhem University Press, Berlin).
merged aquatic vegetation and thus improve
45
ecosystem functioning. Conley (37) further
suggested that if only phosphorus reductions
40
were pursued, i.e. reduce phosphorus such that
35
it is limiting year-round in estuaries, it is likely
30
that the export of nitrogen from those systems
would increase to bordering nitrogen-limited
25
marine systems, thus only exporting the prob20
lem of enhanced production. Unfortunately,
15
our knowledge of the relative importance of nitrogen and phosphorus to phytoplankton
10
growth is focused on temperate systems, and
5
tropical systems, while more frequently limited
0
by phosphorus (103), are less well studied.
0
0.5
1
1.5
2
2.5
3
3.5
The accumulated loads of organic matter and
the internal load of inorganic and organic nuNitrogen fertilizer (Nf), million tonnes yr–1,
trients in the sediments underlying eutrophic
averaged over the 7 years prior to each data point
waters perpetuate conditions of eutrophication
as they continue to be processed by normal
1961–1972
1973
1974–1991
1994–1996
geochemical processes in the sediments (Fig.
9). In addition, there is an inertia in terrestrial
systems and rivers and streams with regard to
110
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Ambio Vol. 31 No. 2, March 2002
by nutrient management schemes that reduced the nitrogen and
phosphorus inputs to the bay (69). Four years after improved
sewage treatment, ambient chlorophyll a concentrations decreased in Hillsborough Bay, and the noxious filamentous
cyanobacteria Schizothrix calcicola also decreased. Modest
seagrass recovery followed. An aggressive nutrient management
program with broad-scale public, institutional, and private participation continues under the Tampa Bay Estuary Program (12).
As a result of the economic collapse of the former Soviet Union and declines in subsidies for fertilizers, the decade of the
1990s witnessed a substantially decreased input of nutrients to
the Black Sea, with resulting signs of recovery in the pelagic
and benthic ecosystems (39). There is a recovery in zoobenthos
species diversity, phytoplankton biomass has declined by about
30% of the 1990 maxima, there is some recovery of the diatoms,
the phytoplankton are more diverse, the incidence of intense
blooms has declined, and there is a limited recovery of some
zooplankton stocks and diversity in limited geographic areas.
There has been no recovery of benthic macroalgae. For the first
time in several decades oxygen deficiency was absent from the
northwestern shelf of the Black Sea in 1996, and receded to an
area less than 1000 km2 in 1999 (Fig. 10). Most fish stocks in
the northwestern Black Sea are still depleted (39). There should
be little doubt of the strong relationships among human activities, Black Sea eutrophication, and demise of pelagic and benthic
coastal ecosystems, as well as similar linkages in the partial recovery of those systems following reduced nutrients. While the
mediator of the nutrient reductions from the watershed of the
Black Sea was economic hardship and decline, i.e., not a preferable means of reducing nutrient loads worldwide, the resilience
of some aspects of the ecosystems within periods of a few years
to a decade is heartening. Researchers within the narrow, coastal
inlets of the Bodden are less optimistic about system recovery
where nutrients to that sector of the Baltic were reduced greatly
during the last decade of the 20th century, but the expected improvement of water quality has not been demonstrated (91).
THE FUTURE
Over the last two decades it has become increasingly apparent
that the effects of excess nutrients and eutrophication in coastal
systems are not minor and localized, but have large-scale implications and are spreading rapidly. Most of these effects are
manifested at the terminus of rivers that traverse temperate landscapes and developed countries, but more evidence has been
documented recently for developing countries (e.g. China, 106),
and especially tropical areas that remain fairly unstudied. The
reasonable concern is that coastal eutrophication historically confined primarily to the temperate zone of the North Atlantic periphery will become a global phenomenon. The responses of terrestrial, freshwater and marine ecosystems to process and transform nitrogen, however, may differ with latitude, temperature
and season, and the overall global dynamics are as yet unpredictable.
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107. I thank the US National Oceanic and Atmospheric Administration, Coastal Ocean Program, for research funds that supported this synthesis, Gene Turner and three anonymous referees for helpful comments on the draft manuscript, and Ben Cole for assistance in preparation of the figures.
Nancy N. Rabalais, PhD, is a professor at the Louisiana
Universities Marine Consortium where she studies the
dynamics of hypoxic environments, interactions of large
rivers with the coastal ocean, estuarine and coastal
eutrophication, benthic ecology, and environmental effects
of habitat alterations and contaminants. Dr. Rabalais is a
AAAS Fellow, an Aldo Leopold Leadership Program Fellow,
a Past President of the Estuarine Research Federation, and
currently the Chair of the Ocean Studies Board of the
National Research Council. Her address: Louisiana
Universities Marine Consortium, 8124 Hwy. 56, Chauvin,
Louisiana 70344, USA.
E-mail: nrabalais@lumcon.edu
© Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
Ambio Vol. 31 No. 2, March 2002