Nitrogen in Aquatic Ecosystems

Author(s): Nancy N. Rabalais

Source: AMBIO: A Journal of the Human Environment, 31(2):102-112. 2002.
Published By: Royal Swedish Academy of Sciences
DOI: http://dx.doi.org/10.1579/0044-7447-31.2.102
URL: http://www.bioone.org/doi/full/10.1579/0044-7447-31.2.102

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological,
and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books
published by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial
inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions,
research libraries, and research funders in the common goal of maximizing access to critical research.
Nancy N. Rabalais
Nitrogen in Aquatic Ecosystems
Aquatic ecosystems respond variably to nutrient enrich-
ment and altered nutrient ratios, along a continuum from
fresh water through estuarine, coastal, and marine sys-
tems. Although phosphorus is considered the limiting
nutrient for phytoplankton production in freshwater sys-
tems, the effects of atmospheric nitrogen and its contri-
bution 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 phyto-
plankton biomass accumulation. There are well-estab-
lished, 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 sys-
tems exceeds the capacity for assimilation of nutrient-
enhanced production, and water-quality degradation oc-
curs. Impacts can include noxious and toxic algal blooms,
increased turbidity with a subsequent loss of submerged
aquatic vegetation, oxygen deficiency, disruption of eco-
system 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 en-
vironmental 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 in-
puts of nitrogen to aquatic ecosystems. It is impossible, how-
ever, 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 sili-
con have remained constant or decreased, often resulting in an
altered stoichiometric balance of nitrogen, phosphorus and sili-
con. 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 re-
main several unresolved issues with regard to the importance of
increased nutrients—in particular, whether there is really an en-
vironmental 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 bal-
ance of necessary and excess nutrients for system productivity,
and what is the potential and time course for recovery of an eco-
102 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
system degraded by excess nutrients given that a suitable nutri-
ent management program is put into place.
NUTRIENT SOURCES AND THEIR CHANGE
Human population growth and its associated activities have al-
tered the landscape, hydrologic cycles, and the flux of nutrients
essential to plant growth at accelerating rates over the last sev-
eral centuries (1, 2). Fossil-fuel consumption and food produc-
tion in support of burgeoning human population growth have in-
creased significantly the flux of nitrogen and phosphorus to
aquatic and terrestrial ecosystems with alterations of global cy-
cles 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 eco-
systems 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 dif-
ferent 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 composi-
tion (e.g. 15, 16).
Phosphorus additions to the landscape enter via phosphorus-
containing fertilizers manufactured from mined phosphorus, ani-
mal 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, phospho-
rus is accumulating in the soil with important implications for
increased runoff from the landscape to surface waters (17). In-
creased flux of phosphorus eroded from the landscape or car-
ried 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 coun-
tries 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, spe-
cifically 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). Phos-
phorus loads, likewise, come mostly from rivers (17, 19). Di-
rect atmospheric deposition of nitrogen and phosphorus on es-
tuaries and coastal waters may contribute as little as 1% to as
much as 30–40% of the total load (20). Clearly there are multi-
ple 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 re-
mained the same or decreased, so that the relative proportions
of silicon to nitrogen and silicon to phosphorus in river efflu-
ents have decreased over time as the nitrogen to phosphorus ra-
Ambio Vol. 31 No. 2, March 2002
 Atmosphere Stratospheric
effects
NOx Ozone PM &
effects visibility
effects Greenhouse
Energy effects
NOx NH3 NH4
production

Food
Figure 1. The nitrogen cascade illustrating the production NHx Crop Animal Forest & grasslands
movement of nitrogen from one effect to
another as it cycles through environmental
reservoirs with emphasis (in red) on flows in Soil Soil
aquatic ecosystems or flows that lead to People
Agroecosystem effects
(food, fiber)
aquatic ecosystems (modified from 1).
Norg
NO3
* *
NO3 NO3
Human activities Groundwater
NO3 effects

NO3
* Terrestrial ecosystems

The
Nitrogen NH4 Lakes, streamwater Coastal
& river effects effects Ocean
Cascade * NO 3 * effects N20
*denitrification Aquatic ecosystems
potential

tio increased (25, 26). The dissolved silicate:nitrate ratio is in-
versely 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 eco-
nomic 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 River-
influenced continental shelf of the Gulf of Mexico (27) and for
the northwestern shelf of the Black Sea affected by a similarly-
altered Danube River (28–30). Shifts of dominant species in
phytoplankton communities as well as an increase in the fre-
quency or size of harmful or noxious algal blooms may also oc-
cur (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 phyto-
plankton 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 nu-
trient 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 ma-
rine ecosystems are probably limited by nitrogen, but phospho-
rus 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
frequent basis (27, 34, 36). Conley (37) reviewed nutrient limi-
tation 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 display-
ing dissolved silicate limitation of the spring diatom bloom.
Similar spatial and seasonal, or longer-term, variability in nu-
trient limitation are apparent in the influence of the Mississippi
and Danube Rivers (38, 39). There is a need to distinguish be-
tween the processes of biomass limitation and growth-rate limi-
tation. If the concern with increased nutrient loads is eutro-
phication, then biomass accumulation is the important issue, and
accumulation of biomass in most coastal marine systems is ni-
trogen 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’ ni-
trogen 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 nu-
trient enrichment.
NUTRIENT-ENHANCED PRODUCTIVITY
Significant positive relationships exist between nutrient-loading
rates and algal production and biomass (13, 44, 45), but non-
linearly 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 lin-
ear regression analysis of river flow (strongly correlated with

Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002 103
http://www.ambio.kva.se
Figure 2. Left panel: the 10 000

Phytoplankton production (g C m–2 yr–1)

relationship between the
input of dissolved
inorganic nitrogen (DIN)
per unit area and primary

Primary production, g C m–2 yr–1

production in a variety of
marine systems (45, with
kind permission of Kluwer 1000
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 100
systems are solid circles.
Right panel: the relation-
ship between annual Annual N loading (mol N m–2 yr–1)
phytoplankton production
vs nitrogen loading of
different coastal areas 10
(from 46 as modified in 0.1 1 10 100
13). Note that data are
presented logarithmically DIN input, mol m–2 yr–1
(left panel) or not (right
panel).

5 5 5
production (g C m–2 d–1)

4 4 4
Mean primary

3 3 3
2 2 2
1 1 1
0 0 0
0 100 200 300 400 0 100 200 300 1 2 3 4 5
NO3 + NO2 flux (106 mol d–1) NO3 + NO2 (µM) Orthophosphate (µM)

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 was demonstrated between river inputs of nitrate and nitrite for
deposition of chlorophyll a, and seasonal declines in deep-wa- other times of the year. Even stronger correlations were observed
ter dissolved oxygen. With appropriate combinations of river between the concentration of orthophosphate and primary pro-
flow (average of current and previous year, flow during winter duction, but these were not significant (smaller sample size).
and spring before deposition of chlorophyll), they demonstrated There was also a high degree of coherence between Mississippi
strong relationships of river flow with primary production and River nitrate flux and net production at a 20-m water depth sta-
the fate of that production. They further demonstrated a strong tion in the core of the hypoxic zone 90 km down-plume from
relationship between the deposition of the production in the form the Mississippi River influence for 1985–1992 (51).
of sedimented chlorophyll a and the seasonal decline of deep- Data from 36 marine systems show a positive relationship be-
water dissolved oxygen. While these relationships do not negate tween fisheries yield and primary production (52) (Fig. 4). On
the importance of water-column stratification and other physi- the other hand, a meta-analysis of 47 marine food webs includ-
cal processes, they do clearly link quantitatively nutrient flux ing open systems (53) indicated that in open systems the avail-
with eventual degradation of water quality in the form of chronic, ability of nitrogen and the primary production rate were strongly
seasonal oxygen deficiency. These same relationships held in an correlated to the accumulation of phytoplankton but not to higher
intra-site comparison within Chesapeake Bay, where overall trophic levels (summarized in 54). Micheli’s analysis (53) dem-
there were strong and linear relationships of primary production, onstrated a weak coupling between phytoplankton, mesoplankton
benthic-pelagic coupling, and nutrient recycling to both fresh- and zooplankton for closed and manipulated systems.
water load and nutrient-loading rates. Grimes (55) pointed out that 70–80% of the Gulf of Mexico
Similar relationships have been identified for the Mississippi fishery landings comes from the water surrounding the Missis-
River-influenced area of the northern Gulf of Mexico continen- sippi River delta, a river that has witnessed a tripling of nitrate
tal shelf where severe seasonal hypoxia develops most summers loads in the last half of the 20th century. While the mechanisms
(42). High biological productivity in the immediate and extended for the apparent enhancement of marine fisheries are not clear,
plume of the Mississippi River is mediated by high nutrient in- he proposed that enhanced recruitment was the most likely proc-
puts and regeneration, favorable light conditions, and suitable ess. Enhanced recruitment, i.e., larval production, feeding,
temperature, salinity, and mixing rates (49, 50). Lohrenz et al. growth and survival, are likely facilitated by both the physical
(47) demonstrated that primary production in shelf waters near characteristics of the river plume (areas of convergence, strati-
the delta and to some distance from it was significantly corre- fication, and transport and retention of fish larvae) and biologi-
lated with nitrate and nitrite concentrations and fluxes over the cal dynamics that favor processes that regulate recruitment. Simi-
period 1988 to 1994 (Fig. 3). Light limitation was likely an im- lar enhancement of fisheries production in Mediterranean wa-
portant factor during winter months, but a positive correlation ters is found in areas under the influence of river effluents (56).

104 © Royal Swedish Academy of Sciences 2002 Ambio Vol. 31 No. 2, March 2002
http://www.ambio.kva.se
 1000 10 There are thresholds, however, where the load of nu-
ESTUARIES ( macrophytes important) trients to a marine system exceeds the capacity for assimi-
SHELF lation, and water-quality degradation occurs with detri-
UPWELLING mental effects on components of the ecosystem and on
OTHER MARINE ecosystem functioning. Caddy (57) illustrated how an in-
AFRICAN LAKES (Melack 1976) crease in nutrient input results in a continuum of fisher-
ies 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 ef-
100 1.0
fects of eutrophication, such as the loss of seabed veg-
etation and extensive bottom-water oxygen depletion is
complicated by poor fisheries data, inadequate economic
Fisheries, kg ha–1 yr–1

indicators, increase in overharvesting that occurred at the

g C m–2 yr–1
1%

time that habitat degradation progressed, natural variabil-

ity of fish populations, shifts in harvestable populations,
and climatic variability (14, 56, 58, 59). Eutrophication
of surface waters accompanied by oxygen deficient bot-
tom waters can lead to a shift in dominance of fish stocks
from demersals to pelagics. In the Baltic Sea and Kattegatt
10 0.1 where eutrophication-related ecological changes occurred
mainly after World War II (60), changes in fish stocks
36 MARINE have been both positive, due to increased food supply (e.g.
SYSTEMS
r–1 = 0.84 pike perch in Baltic archipelagos) and negative (e.g. oxy-
gen deficiency reducing Baltic cod recruitment and even-
tual harvest). Similar shifts are hinted at with limited data
on the Mississippi River-influenced shelf with the increase
OGLESBY (1977) in selected pelagic species in bycatch from shrimp trawls
r–2 . 0.74
15 LAKES > 10 km2 and a decrease in certain demersal species (61). In the case
of commercial fisheries in the Black Sea, it is difficult to
0
discern the impact of eutrophication through the loss of
0 100 1000 macroalgal habitat and oxygen deficiency or a shift in the
Primary production, g C m–2 yr–1 system from dominance by benthic production to pelagic
Figure 4. Relationship between fisheries yield per unit area and primary production as eutrophication advanced, amid the possibil-
production per unit area across a spectrum of aquatic ecosystems (52). ity of overfishing. After the mid-1970s, benthic fish
The r2 for regressions for marine systems and freshwater lakes are populations (e.g. turbot) collapsed, and pelagic fish
superimposed. (Publ. with kind permission of the American Association
of Limnology and Oceanography).

Figure 5. The generalized

relationship of
production and fishery
yield as nutrient loading
increases with varying
effects of eutrophication
expressed as seasonal
and permanent bottom-
water anoxia; a spectrum
of enclosed seas
(modified from 13, with
kind permission of Inter-
Research Science
Publisher).

Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002 105
http://www.ambio.kva.se
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 en-
vironmental problems that lead to decreased landings or reduced
quality of production and biomass.
NUTRIENT ENRICHMENT ALONG THE FRESH-
WATER TO MARINE CONTINUUM
The effects of nitrogen enrichment in the environment are nu-
merous, including both beneficial and detrimental, as the vari-
ous 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 com-
ponent 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 re-
sult of increased nitrogen and phosphorus inputs, but could re-
sult from the supply of excessive decomposable organic carbon
as well.
Where excess carbon is produced and accumulates, second-
ary 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 deg-
radation 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 exam-
ples of localized or temporary loss of biodiversity, shifts in com-
munity structure in both pelagic and benthic systems, and de-
graded habitats, such as coral reefs, seagrass beds, and produc-
tive 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).
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 sev-
eral 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 trans-
formed through microbial processes in soils to biologically avail-
able nitrogen in ground and surface waters, there are a number
of effects beginning with groundwater contamination and sur-
face-water acidification.
Freshwater systems that are poorly buffered by surrounding
soils can be acidified by increased deposition of nitrate and am-
monium. The continuing acidification of Europe, northeastern
North America and parts of Asia is now increasingly a nitro-
gen-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
106 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
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 acidifi-
cation enhances mercury accumulation in fish. Acidification of
surface waters results in a decrease in the survival, size, and den-
sity of fish and in the loss of fish and other aquatic biota from
lakes and streams.
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 phyto-
plankton, 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 de-
crease in the penetration of light through the water column. Well-
documented examples of decline in Secchi disk depth with in-
creases in nutrient loads to coastal systems exist for the north-
ern 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 sub-
merged 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 vegeta-
tion or increase the incidence of drifting macroalgae (68). Typi-
cal of nutrient-enriched temperate and tropical regions are ‘nui-
sance’ macroalgae, typically the filamentous or sheet-like forms
(Ulva, Cladophora, Chaetomorpha, Gracilaria) that accumulate
in extensive, thick unattached mats over seagrasses or the sedi-
ment 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 de-
crease of light availability for photosynthetic, oxygen-produc-
ing 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 in-
dustrial sources. Obvious signs of eutrophication in Tampa Bay
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)
4
2
0
1980 1984 1988 1992 1996
Year
Ambio Vol. 31 No. 2, March 2002
were high turbidity, anoxia of bottom waters, large amounts of
drift macroalgae in the shallows, and loss of most of the sub-
merged 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). Pro-
longed 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 suspen-
sion-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 spe-
cies as eutrophication increases (72) (Fig. 7). i) In uneutrophied
marine or brackish shallow coastal waters, the dominant produc-
ers 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 eutro-
phication, increased nutrient loading favors the growth of bloom-
forming phytoplankton and fast-growing, short-lived epiphytic
macroalgae over slow-growing, long-lived macrophytes. Phan-
erogams and perennial macroalgal communities gradually de-
cline along with changes in the structure (species composition,
coverage, or depth distribution limits) and their function (pro-
duction and reproduction). iii) With increased nutrient loads to-
wards 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 con-
ditions, phytoplankton constitute the dominant primary produc-
ers and benthic macrophytes disappear completely. This se-
quence 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 in-
creased nutrient levels. Similarly, data from joint nutrient enrich-
ment 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 spawn-
ing 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 com-
promised 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).
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 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
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 Relative dominance
epiphytes of primary producers
Free floating
macroalgae
Perennial benthic
macrophytes
Phytoplankton
B
Light
penetration
Relative levels of chemical
and physical parameters Nutrient
level
Stable
Increasing
substrate
Resuspension
and indirectly cause impacts through the consumption of toxins
accumulated in fish and shellfish. Less obvious impacts are re-
duced grazing, increased flux of organic matter leading to hy-
poxia, and changes in trophic dynamics.
There has been some debate as to whether the frequency of
harmful algal blooms has increased, but several researchers sug-
gest a clear global expansion (77). Temporal trajectories of in-
creased occurrence of HABs with increased nutrient loads are
repeatable worldwide, but other factors, such as increased aware-
ness 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 harm-
ful algal blooms in the Seto Inland Sea, Japan (78). Red-tide out-
break 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 sub-
sequent 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 eutro-
phication to several HAB species (79). Harmful algal blooms,
in general, however, cannot always be linked to nutrient over-
enrichment.
Nutrient enrichment (both nitrogen and phosphorus) of fresh
and brackish environs leads to increasing blooms of cyano-
bacteria 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 ni-
trogen-enriched water from the Mississippi River (81). Pfiesteria
piscicida, a dinoflagellate responsible for massive fish kills in
Pamlico-Albemarle Sound, North Carolina and serious neuro-
logical human health risks, is associated with high organic load-
ing 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
107
appears to have increased dramatically since the 1950s coinci-
dent with human-related increases in riverine nitrogen flux (86,
87). Thus, there is evidence for the linkage of nutrient over-
enrichment to some toxic forms that kill or debilitate higher or-
ganisms 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 car-
bon 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 oxy-
gen during the decay of the carbon and deplete the oxygen in
the lower water column at a faster rate than the diffusion of oxy-
gen 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 Rosen-
berg (63), however, there was a consistent trend of increasing
severity (either duration, intensity, or size) where hypoxia oc-
curred 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 ad-
jacent 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 overenrich-
ment. 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 bottom-
water hypoxia distribution). Hypoxia existed on the northwest-
ern 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).
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 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
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 recov-
ery occurs, recurring on a seasonal basis, or permanent so that
long-term ecosystem structure and function shifts. As the oxy-
gen concentration falls from saturated or optimal levels towards
depletion, a variety of behavioral and physiological impair-
ments affect the animals that reside in the lower water column
or in the sediments or attached to hard substrates. Mobile ani-
mals, such as shrimp, fish, and some crabs, flee waters where
the oxygen concentration falls below 3 to 2 mg L–1. As dis-
solved oxygen concentrations continue to fall, less mobile or-
ganisms 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 equi-
librium species such as long-lived bivalves and a greater domi-
nance of short-lived surface-dwelling forms (89). Long-term
trends for the Skagerrak coast of western Sweden in semi-en-
closed fjordic areas experiencing increased oxygen stress (90)
showed declines in the total abundance and biomass of macro-
infauna, abundance and biomass of mollusks, and abundance
of suspension feeders and carnivores. These changes in benthic
communities result in an impoverished diet for bottom-feed-
ing fish and crustaceans and contribute, along with low dis-
solved oxygen, to altered sediment biogeochemical cycles.
As aerobic bacteria decompose the increased organic matter
settling onto the seabed and the dissolved oxygen concentra-
tion overlying the sediments approaches anoxia, numerous bio-
logical 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 bio-
mass, microbial decomposition potential of substrates, and com-
munity oxygen consumption increase, but not in simple linear
relationships (91). The redox potential discontinuity layer mi-
grates upward to the sediment-water interface, sulfate respira-
tion replaces oxygen respiration, hydrogen sulfide is generated
from the sediments, and oxygen penetrates less deeply into
the sediments as the bioturbation potential of the macro-
infauna decreases during their demise due to sulfide toxicity
or lack of sufficient oxygen. The sediments become less cohe-
sive, more susceptible to resuspension, and contribute to tur-
Ambio Vol. 31 No. 2, March 2002
Figure 9. Interactions of nitrogen and
phosphorus cycling in oxic vs anoxic Overlaying water
sediments (modified from 105, with kind
permission from the Dalhem Workshop
Report “Science and Integrated Coastal
Management”, Dalhem University Press).
bidity of the overlying water, which in turn reduces the poten-
tial for growth of the photosynthetic microphytobenthic commu-
nity and generation of oxygen into the lower water column. Some
shifts in the benthic microbial community are visible at the sedi-
ment-water interface. Typical black spots from iron sulfide pre-
cipitated from intense microbial degradation of organic matter,
lacey white colonies and denser, yellowish colonies of sulfur-
oxidizing bacteria (Beggiatoa spp. and Thiovulum sp.), and red-
dish to violet carpets of sulfur-purple bacteria can be observed
as oxygen levels decline in the Wadden Sea (North Sea), in shal-
low water areas of the Baltic, on the Louisiana continental shelf,
and many areas of the world’s ocean where the oxygen mini-
mum zone intersects the seabed (14).
Several microbially-mediated processes in sediments at the
surface of the seabed are altered as overlying waters become an-
oxic, often with negative feedback loops to continued degrada-
tion 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 con-
centration, there is an increase in the flux of inorganic nutrients,
ammonium and particularly phosphate, into the overlying wa-
ter. 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 world-
wide (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 wa-
ters surrounding many coral reefs. Direct destruction in construc-
tion 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 aggra-
vated 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 con-
Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
Organic matter Organic matter
Lost from
system
Recycled
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 diver-
sion, D. cavernosa cover on reef slopes decreased substantially
in southern Kaneohe Bay, the site of most of the historical sew-
age 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 surround-
ing waters. The intensive ENCORE experiment (Enrichment of
Nutrients on a Coral Reef Experiment) on 12 pristine coral at-
olls of the Great Barrier Reef (98) demonstrated that reef organ-
isms and processes were impacted by elevated nutrients, that
impacts included positive responses, that impacts were depend-
ent on dose level, whether nitrogen and/or phosphorus were el-
evated, 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 con-
troversial. The discourse on this controversy promises to con-
tinue for some time.
Nutrient effects on coral reefs are likely to be more evident
in bays and confined water-bodies rather than well-flushed oce-
anic reefs. Nutrients are probably less important than other fac-
tors 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 in-
fluences, atmospheric and advective (upwelling/deep mixing)
nutrient inputs may be the key sources of ‘new’ nutrients sup-
porting primary production. Both wet and dry atmospheric depo-
sition contain various biologically reactive nitrogen forms, and
109
atmospheric deposition of continental dust is the primary source
of new iron to the oceans. In a review of atmospherically-de-
rived nitrogen as ‘new’ nitrogen inputs in diverse estuarine,
coastal and open-ocean waters, Paerl et al. (20) compiled esti-
mated 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 Sar-
gasso 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 experi-
ments on offshore and Gulf Stream waters off North Carolina
and Sargasso Sea waters with a series of nitrogen forms, phos-
phate, 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 natu-
ral 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 fixa-
tion by the nitrogen-fixing cyanobacteria Tricho-
desmium. 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 hydrologi-
cal cycle. Lenes et al. (102) note the stimulatory effect of sum-
mer delivery of iron in the form of Saharan dust to the
oligotrophic waters of the eastern Gulf of Mexico in stimulat-
ing Trichodesmium blooms there over the last 50 years, and fur-
ther point out the potential connection between regenerated ni-
trogen forms from the blooms and the stimulation of blooms of
the toxic dinoflagellate Gymnodinium breve (= Karenia brevis).
RECOVERY AND NUTRIENT MANAGEMENT
Howarth (8) noted that, given our understanding of nutrient limi-
tation and knowledge of increasing inputs of nutrients to coastal
systems, to control eutrophication in these systems requires ni-
trogen 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 con-
centrations. Reductions in nitrogen loading
should reduce summer chlorophyll concentra- Figure 10. The relationship of nitrogen loads to the northwestern shelf of the Black Sea vs
tions and improve the conditions for sub- the size of the bottom-water hypoxic zone for the periods indicated (39, with kind
permission of Dalhem University Press, Berlin).
merged aquatic vegetation and thus improve
ecosystem functioning. Conley (37) further 45
suggested that if only phosphorus reductions 40
were pursued, i.e. reduce phosphorus such that
35
Thousands of km2 of
it is limiting year-round in estuaries, it is likely
hypoxia (km2 . 103)
that the export of nitrogen from those systems 30
would increase to bordering nitrogen-limited 25
marine systems, thus only exporting the prob-
20
lem of enhanced production. Unfortunately,
our knowledge of the relative importance of ni- 15
trogen and phosphorus to phytoplankton 10
growth is focused on temperate systems, and 5
tropical systems, while more frequently limited
by phosphorus (103), are less well studied. 0
The accumulated loads of organic matter and 0 0.5
the internal load of inorganic and organic nu-
trients in the sediments underlying eutrophic
waters perpetuate conditions of eutrophication
as they continue to be processed by normal
geochemical processes in the sediments (Fig.
9). In addition, there is an inertia in terrestrial
systems and rivers and streams with regard to
110 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
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 eas-
ily 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 projec-
tion 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 agricul-
ture, or to trap the nutrients in the watershed by wetland and
riparian-zone restoration. Assessing whether the reduction tar-
gets were reached was difficult, but it appears that the goal was
nearly met for phosphorus, but nitrogen loadings, although re-
duced, 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 de-
crease in the use of commercial fertilizers that started in the late
1980s. In western Europe, while studies of decreased phospho-
rus emissions have shown that riverine phosphorus loads can be
rapidly reduced from high to moderate levels, a further reduc-
tion, if achieved at all, may take decades.
Within estuaries and coastal systems, decrease in external nu-
trient 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 nu-
trients. Boynton and Kemp (48) suggested a ‘nutrient memory’
over time scales of a year rather than seasonal periods as sug-
gested 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 cov-
erage is only a small portion of the habitat occupied in the 1950s
(105). Justić et al. (51) suggested that at least a year of contin-
ued carbon respiration following high deposition of carbon in a
flood year contributed to oxygen demand on the Louisiana con-
tinental shelf in the subsequent summer.
The severe degradation of water quality in Tampa Bay and
loss of valuable habitat, particularly seagrass beds, was followed
1 1.5 2 2.5 3 3.5
Nitrogen fertilizer (Nf), million tonnes yr–1,
averaged over the 7 years prior to each data point
1961–1972 1973 1974–1991 1994–1996
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 de-
creased 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 par-
ticipation continues under the Tampa Bay Estuary Program (12).
As a result of the economic collapse of the former Soviet Un-
ion 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 activi-
ties, Black Sea eutrophication, and demise of pelagic and benthic
coastal ecosystems, as well as similar linkages in the partial re-
covery of those systems following reduced nutrients. While the
References and Notes
1. Vitousek, P.M., Aber, J.D., Howarth, R.W., Likens, G.E., Matson, P.A., Schindler,
D.W., Schlesinger, W.H. and Tilman, D.G. 1997. Human alterations of the global ni-
trogen cycle: Sources and consequences. Ecol. Appl. 7, 737–750.
2. Galloway, J.N. and Cowling, E.B. 2002. Nitrogen and the world. Ambio 31, 64–71.
3. Schindler, D.W. 1978. Factors regulating phytoplankton production and standing crop
in the world’s freshwaters. Limnol. Oceanogr. 23, 478–486.
4. Hecky, R.E. and Kilham, P. 1988. Nutrient limitation of phytoplankton in freshwater
and marine environments: a review of recent evidence on the effects of enrichment.
Limnol. Oceanogr. 33, 796–822.
5. Smetacek, V., Bathman, U., Nothig, E.M. and Scharek, R. 1991. Coastal eutrophication:
causes and consequences. In: Ocean Margin Processes in Global Change. Mantoura,
R.F.C., Martin, J.M. and Wollast, R. (eds). John Wiley and Sons, New York, pp. 251–
279.
6. Vollenweider, R.A., Marchetti, R. and Viviani, R. (eds). 1992. Marine Coastal
Eutrophication. The Response of Marine Transitional Systems to Human Impact: Prob-
lems and Perspectives for Restoration. Proceedings, International Conference, Bo-
logna, Italy, 21–24 March 1990. Elsevier, Amsterdam, The Netherlands.
7. Nixon, S.W. 1995. Coastal marine eutrophication: A definition, social causes, and fu-
ture concerns. Ophelia 41, 199–219.
8. Howarth, R.W. 1988. Nutrient limitation of net primary production in marine ecosys-
tems. Ann. Rev. Ecol. System. 19, 898–910.
9. Howarth, R.W., Jensen, H., Marino, R. and Postma, H. 1995. Transport to and process-
ing of P in near-shore and oceanic waters. In: Phosphorus in the Global Environment:
Transfers, Cycles and Management. Tiessen, H. (ed.). SCOPE 54, Wiley, Chichester,
UK, pp. 323–345.
10. Howarth, R.W., Billen, G., Swaney, D., Townsend, A., Jaworski, N., Lajtha, K., Down-
ing, J.A., Elmgren, R., Caraco, N., Jordan, T., Berendse, F., Freney, J., Kudeyarov,
V., Murdoch, P. and Zhao-Liang, Z. 1996. Regional nitrogen budgets and riverine N
& P fluxes for the drainages to the North Atlantic Ocean: natural and human influ-
ences. Biogeochemistry 35, 75–139.
11. Jørgensen, B.B. and Richardson, K. (eds). 1996. Eutrophication in Coastal Marine
Ecosystems. Coastal and Estuarine Studies 52, American Geophysical Union, Wash-
ington, D.C., 267 pp.
12. National Research Council (NRC Committee on the Causes and Management of
Coastal Eutrophication, Ocean Studies Board and Water Science and Technology
Board) 2000. Clean Coastal Waters. Understanding and Reducing the Effects of Nu-
trient Pollution. National Academy Press, Washington, D.C., 393 pp.
13. Cloern, J.E. 2001. Review. Our evolving conceptual model of the coastal eutrophication
problem. Mar. Ecol. Prog. Ser. 210, 223–253.
14. Rabalais, N.N. and Turner. R.E. (eds). 2001. Coastal Hypoxia: Consequences for Living
Resources and Ecosystems. Coastal and Estuarine Studies 58, American Geophysical
Union, Washington, D.C., 454 pp.
15. Antia, N., Harrison, P. and Oliveira, L. 1991. The role of dissolved organic nitrogen
in phytoplankton nutrition, cell biology, and ecology. Phycologia 30, 1–89.
16. Peierls, B. and Paerl, H. 1997. Bioavailability of atmospheric organic nitrogen depo-
sition to coastal phytoplankton. Limnol. Oceanogr. 42, 1819-1823.
17. Bennett, E.M., Carpenter, S.R. and Caraco, N.F. 2001. Human impact on erodable
phosphorus and eutrophication: a global perspective. BioScience 51, 227–234.
18. Goolsby, D.A., Battaglin, W.A., Lawrence, G.B., Artz, R.S., Aulenbach, B.T., Hooper,
R.P., Keeney, D.R. and Stensland, G.J. 1999. Flux and Sources of Nutrients in the
Mississippi-Atchafalaya River Basin, Topic 3 Report for the Integrated Assessment of
Hypoxia in the Gulf of Mexico. NOAA Coastal Ocean Program Decision Analysis Se-
ries No. 17, NOAA Coastal Ocean Program, Silver Springs, Maryland, 130 pp.
19. Grimvall, A. and Stålnacke, P. 2001. Riverine inputs of nutrients to the Baltic Sea.
In: A Systems Analysis of the Baltic Sea. Wulff, F.V., Rahm, L.A. and Larsson, P.
(eds). Ecological Studies Analysis and Synthesis, Vol.148, Springer, Berlin, pp. 113–
131.
20. Paerl, H.W., Boynton, W.R., Dennis, R.L., Driscoll, C.T., Greening, H.S., Kremer,
J.N., Rabalais, N.N. and Seitzinger, S.P. 2000. Atmospheric deposition of nitrogen in
coastal waters: biogeochemical and ecological implications. In: Nitrogen Loading in
Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
mediator of the nutrient reductions from the watershed of the
Black Sea was economic hardship and decline, i.e., not a pref-
erable 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 im-
provement 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 im-
plications and are spreading rapidly. Most of these effects are
manifested at the terminus of rivers that traverse temperate land-
scapes 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 con-
fined primarily to the temperate zone of the North Atlantic pe-
riphery will become a global phenomenon. The responses of ter-
restrial, freshwater and marine ecosystems to process and trans-
form nitrogen, however, may differ with latitude, temperature
and season, and the overall global dynamics are as yet unpre-
dictable.
Coastal Water Bodies. An Atmospheric Perspective. Valigura, R.A., Alexander, R.B.,
Castro, M.S., Meyers, T.P., Paerl, H.W., Stacey, P.E. and Turner, R.E. (eds). Coastal
and Estuarine Studies 57, American Geophysical Union, Washington, D.C., pp. 11-
53.
21. Bradley, M.J. and Jones, B.M. 2002. Reducing global NOX emissions: promoting the
development of advanced energy and transportation technologies. Ambio 31, 141–149.
22. Cassman, K.G., Dobberman, A. and Walters, D. 2002. Agroecosystems, nitrogen-use
efficiency, and nitrogen management. Ambio 31, 132–140.
23. Melillo, J.M. and Cowling, E.B. 2002. Reactive nitrogen and public policies for envi-
ronmental protection. Ambio 31, 150–158.
24. Oenema, O. and Pietrzak, S. 2002. Nutrient management in food production; achiev-
ing agronomic and environmental targets. Ambio 31, 159–168.
25. Justić, D., Rabalais, N.N. and Turner, R.E. 1995. Stoichiometric nutrient balance and
origin of coastal eutrophication. Mar. Pollut. Bull. 30, 41–46.
26. Turner, R.E., Rabalais, N.N., Justić, D. and Dortch, Q. Global patterns of dissolved
N, P and Si in large rivers. Biogeochemistry: (In press).
27. Turner, R.E., Qureshi, N., Rabalais, N.N., Dortch, Q., Justić, D., Shaw, R.F. and Cope,
J. 1998. Fluctuating silicate:nitrate ratios and coastal plankton food webs. Proc. Natl
Acad. Sci., USA 95, 13048–13051.
28. Zaitsev, Y.P. 1992. Recent changes in the trophic structure of the Black Sea. Fish.
Oceanogr. 1, 180–189.
29. Tolmazin, R. 1985. Changing coastal oceanography of the Black Sea. I. Northwest-
ern shelf. Progr. Oceanogr. 15, 2127–276.
30. Humborg, C., Ittekkot, V., Caciasu, A. and von Bodungen, B. 1997. Effect of Dan-
ube River dam on Black Sea biogeochemistry and ecosystem structure. Nature 386,
385–388.
31. Officer, CB. and Ryther, J.H. 1980. The possible importance of silicon in marine
eutrophication. Mar. Ecol. Prog. Ser. 3, 83–91.
32. Smayda, T.J. 1990. Novel and nuisance phytoplankton blooms in the sea: evidence
for a global epidemic. In: Toxic Marine Phytoplankton. Granéli, E., Anderson, D.M.,
Edler, L. and Sundstrøm, B.G. (eds). Elsevier Science Publishing Co., Inc., New York,
pp. 29–40.
33. Vitousek, P.M. and Howarth, R.W. 1991. Nitrogen limitation on land and in the sea:
how can it occur? Biogeochemistry 13, 87–115.
34. Conley, D.J., Schelske, C.L. and Stoermer, E.F. 1993. Modification of the biogeo-
chemical cycle of silica with eutrophication. Mar. Ecol. Prog. Ser. 101, 179–192.
35. Ryther, J.H. and Dunstan, W.M. 1971. Nitrogen, phosphorus, and eutrophication in
the coastal marine environment. Science 171, 1008–1013.
36. Dortch, Q. and Whitledge, T.E. 1992. Does nitrogen or silicon limit phytoplankton
production in the Mississippi River plume and nearby regions? Cont. Shelf Res. 12,
1293–1309.
37. Conley, D.J. 2000. Biogeochemical nutrient cycles and nutrient management strate-
gies. Hydrobiologia 410, 87–96.
38. Rabalais, N.N., Turner, R.E., Justić, D., Dortch, Q. and Wiseman, Jr. W.J. 1999. Char-
acterization of Hypoxia: Topic 1 Report for the Integrated Assessment of Hypoxia in
the Gulf of Mexico. NOAA Coastal Ocean Program Decision Analysis Series No. 15.
NOAA Coastal Ocean Program, Silver Spring, Maryland, 167 pp.
39. Mee, L.D. 2001. Eutrophication in the Black Sea and a basin-wide approach to its
control. In: Science and Integrated Coastal Management. von Bodungen, B. and
Turner, R.K. (eds). Dahlem University Press, Berlin, pp. 71–91.
40. Malone, T.C., Conley, D.J., Fisher, T.R., Glibert, P.M., Harding, L.W. and Sellner,
K.G. 1996. Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay.
Estuaries 19, 371–385.
41. Harding, Jr., L.W. and Perry, E.S. 1997. Long-term increase of phytoplankton biomass
in Chesapeake Bay, 1950–1994. Mar. Ecol. Prog. Ser. 157, 39–52.
42. Rabalais, N.N., Turner, R.E., Dortch, Q., Justić, D., Bierman, Jr. V.J. and Wiseman,
Jr., W.J. 2002. Review. Nutrient-enhanced productivity in the northern Gulf of Mexico:
Past, present and future. Hydrobiologia: in press.
43. Zehr, J.P., Waterbury, J.B., Turner, P.J., Montoya, J.P., Osmoregie, E., Steward, G.F.,
Hansen, A. and Karl, D.M. 2001. Unicellular cyanobacteria fix N2 in the subtropical
111
 North Pacific Ocean. Nature 412, 635–638.
44. Boynton, W.R., Kemp, W.M. and Keefe, C.W. 1982. A comparative analysis of nu-
trients and other factors influencing estuarine phytoplankton production. In: Estua-
rine Comparisons. Kennedy, V.S. (ed.). Academic Press, New York, pp. 69–90.
45. Nixon, S.W., Ammerman, J.W., Atkinson, L.P., Berounsky, V.M., Billen, G., Boicourt,
W.C., Boynton, W.R., Church, T.M., DiToro, D.M., Elmgren, R., Garber, J.H., Giblin,
A.E., Jahnke, R.A., Owens, N.J.P., Pilson, M.E.Q. and Seitzinger, S.P. 1996. The fate
of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Bio-
geochemistry 35, 141–180.
46. Borum, J. 1996. Shallow waters and land/sea boundaries. In: Eutrophication in Coastal
Marine Ecosystems. Jørgensen, B.B. and Richardson, K. (eds), Coastal and Estuarine
Studies 52, American Geophysical Union, Washington, D.C., pp. 179–203.
47. Lohrenz, S.E., Fahnenstiel, G.L., Redalje, D.G., Lang, G.A., Chen, X. and Dagg, M.J.
1997. Variations in primary production of northern Gulf of Mexico continental shelf
waters linked to nutrient inputs from the Mississippi River. Mar. Ecol. Prog. Ser. 155,
435–454.
48. Boynton, W.R. and Kemp, W.M. 2000. Influence of river flow and nutrient loads on
selected ecosystem processes. A synthesis of Chesapeake Bay data. In: Estuarine Sci-
ence: A Synthesis Approach to Research and Practice. Hobbie, J.E. (ed.). Island Press,
Washington, D.C., pp. 269–298.
49. Lohrenz, S.E., Dagg, M.J. and Whitledge, T.E. 1990. Enhanced primary production
at the plume/oceanic interface of the Mississippi River. Cont. Shelf Res. 10, 639–664.
50. Lohrenz, S.E., Fahnenstiel, G.L. and Redalje, D.G. 1994. Spatial and temporal varia-
tions in photosynthesis parameters in relation to environmental conditions in coastal
waters of the northern Gulf of Mexico. Estuaries 17, 779–795.
51. Justić, D., Rabalais, N.N. and Turner, R.E. 1997. Impacts of climate change on net
productivity of coastal waters: Implications for carbon budget and hypoxia. Climate
Res. 8, 225–237.
52. Nixon, S.W. 1988. Physical energy inputs and the comparative ecology of lake and
marine ecosystems. Limnol. Oceanogr. 33, 1005–1025.
53. Micheli, F. 19999. Eutrophication, fisheries, and consumer-resource dynamics in ma-
rine pelagic ecosystems. Science 285, 1396–1399.
54. Turner, R.E. 2001. Some effects of eutrophication on pelagic and demersal marine
food webs. In: Coastal Hypoxia: Consequences for Living Resources and Ecosystems.
Rabalais, N.N. and Turner, R.E. (eds). American Geophysical Union, Coastal and Es-
tuarine Studies 58, pp. 371–398.
55. Grimes, C.B. 2001. Fishery production and the Mississippi River discharge. Fisher-
ies 26, 17–26.
56. Caddy, J.F. 2000. Marine catchment basin effects versus impacts of fisheries on semi-
enclosed seas. ICES J. Mar. Sci. 57, 628–640.
57. Caddy, J.F. 1993. Toward a comparative evaluation of human impacts on fishery eco-
systems of enclosed and semi-enclosed seas. Rev. Fish. Sci. 1, 57–95.
58. Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque,
B.J., Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S.,
Lange, C.B., Warner, R.R., et al. 2001. Historical overfishing and the recent collapse
of coastal ecosystems. Science 293, 629–638.
59. Boesch, D.F., Burreson, E., Dennison, W., Houde, E. Kemp, M., Kennedy, V., Newell,
R., Paynter, K., Orth, R. and Ulanowicz. 2001. Factors in the decline of coastal eco-
systems. Science 293, 1589–1590.
60. Elmgren, R. and Larsson, U. 2001. Eutrophication in the Baltic Sea area. Integrated
coastal management issues. In: Science and Integrated Coastal Management. von
Bodungen, B. and Turner, R.K. (eds). Dahlem University Press, Berlin, pp. 15–35.
61. Chesney, E.J. and Baltz, D.M. 2001. The effects of hypoxia on the northern Gulf of
Mexico coastal ecosystem: A fisheries perspective. In: Coastal Hypoxia: Consequences
for Living Resources and Ecosystems. Rabalais, N.N. and Turner, R.E. (eds). Ameri-
can Geophysical Union, Coastal and Estuarine Studies 58, pp. 321–354.
62. Rosenberg, R. 1985. Eutrophication-the future marine coastal nuisance? Mar. Pollut.
Bull. 16, 227–231.
63. Diaz, R.J. and Rosenberg, R. 1995. Marine benthic hypoxia: A review of its ecologi-
cal effects and the behavioural responses of benthic macrofauna. Ocean. Mar. Biol.
Ann. Rev. 33, 245–303.
64. Smith, V.H., Tilman, G.D. and Nekola, J.C. 1999. Eutrophication: impacts of excess
nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ. Pollut. 100,
179–196.
65. Matson, P., Lohse, K. and Hall, S.J. 2002. The globalization of nitrogen: consequences
for terrestrial ecosystems. Ambio 31, 113–119.
66. Driscoll, C.T., Lawrence, G.B., Bulger, A.J., Butler, T.J., Cronan, C.S., Eagar, C., Lam-
bert, K.F., Likens, G.E., Stoddard, J.L. and Weathers, K.C. 2001. Acidic deposition
in the northeastern United States: Sources and inputs, ecosystem effects, and man-
agement strategies. BioScience 51, 180–198.
67. Justić, D. 1988. Trend in the transparency of the northern Adriatic Sea 1911–1982.
Mar. Pollut. Bull. 19, 32–35.
68. McGlathery, K.J. 2001. Macroalgal blooms contribute to the decline of seagrass in
nutrient-enriched coastal waters. J. Phycol. 37, 453–456.
69. Johansson, J.O.R. and Lewis III, R.R. 1992. Recent improvements of water quality
and biological indicators in Hillsborough Bay, a highly impacted subdivision of Tampa
Bay, Florida, USA. In: Marine Coastal Eutrophication. The Response of Marine Tran-
sitional Systems to Human Impact: Problems and Perspectives for Restoration, Pro-
ceedings, International Conference, Bologna, Italy, 21–24 March 1990. Vollenweider,
R.A., Marchetti, R. and Viviani, R. (eds), Elsevier, Amsterdam, pp. 1199–11215.
70. Bricelj, V.M. and Lonsdale, D.J. 1997. Aureococcus anophagefferens: Causes and eco-
logical consequences of brown tides in US mid-Atlantic coastal waters. Limnol.
Oceanogr. 42, 1023–1038.
71. Stockwell, D.A., Whitledge, T.E., Buskey, E.J., DeYoe, H., Dunton, K.C., Holt, G.J.
and Holt, S.A. 1996. Texas coastal lagoons and a persistent brown tide. In: Brown
Tide Summit, Ronkonkoma, NY (USA, 20–21 Oct 1995). McElroy, A. (ed.). New
York Sea Grant Program Publ. No. NYSGI-W-95-001, pp. 81–85.
72. Schramm, W. 1999. Factors influencing seaweed responses to eutrophication: some
results from EU-project EUMAC. J. Appl. Phycol. 11, 69–78.
73. Heck, Jr. K.L., Pennock, J.R., Valentine, J.F., Coen, L.D. and Sklenar, S.A. 2000. Ef-
fects of nutrient enrichment and small predator density on seagrass ecosystems: An
experimental assessment. Limnol. Oceanogr. 45, 1041–1057.
74. Jansson, B.-O. and Dahlberg, K. 1999. The environmental status of the Baltic Sea in
the 1940s, today, and in the future. Ambio 28, 312–319.
75. Sandén, P. and Håkansson, B. 1996. Long-term trends in Secchi depth in the Baltic
Sea. Limnol. Oceanogr. 41, 346–351.
76. Kautsky, N., Kautsky, H., Kautsky, U. and Waern, M. 1986. Decreased depth pen-
etration of Fucus vesiculosus (L.) since the 1940’s indicates eutrophication of the Baltic
Sea. Mar. Ecol. Prog. Ser. 28, 1–8.
77. Anderson, D.M., Glibert, P.M. and Burkholder, J.M. 2002. Harmful algal blooms and
eutrophication: nutrient sources, composition, and consequences. Estuaries: in press.
78. Cherfas, J. 1990. The fringe of the ocean-under siege from land. Science 248, 163–
165.
79. Burkholder, J.M. 1998. Implications of harmful microalgae and heterotrophic
dinoflagellates in management of sustainable marine fisheries. Ecol. Appl. 8 Suppl.,
37–62.
80. Paerl, H.W. 1996. A comparison of cyanobacterial bloom dynamics in freshwater, es-
112 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
tuarine and marine environments. Phycologia 35, 25–35.
81. Dortch, Q., Peterson, T.D. and Acheé, S. 1999. The 1997 algal bloom in Lake
Pontchartrain. In: Effects of the 1997 Bonnet Carré Opening on Nutrients and Phyto-
plankton in Lake Pontchartrain. Turner, R.E., Dortch, Q. and Rabalais N.N. (eds).
Report to Lake Pontchartrain Basin Foundation, Metairie, Louisiana, pp. 6.1–6.20.
82. Burkholder, J.M. and Glasgow, Jr. H.B. 1997. Pfiesteria piscicida and other Pfiesteria-
like dinoflagellates: behavior, impacts, and environmental controls. Limnol. Oceanogr.
42, 1052–1075.
83. Burkholder, J.M., Glasgow, Jr. H.B. and Hobbs, C.W. 1995. Fish kills linked to a toxic
ambush-predator dinoflagellate: Distribution and environmental conditions. Mar. Ecol.
Prog. Ser. 124, 43–61.
84. Parsons, M.L., Scholin, C.A., Miller, P.E., Doucette, G.J., Powell, C.L., Fryxell, G.A.,
Dortch, Q. and Soniat, T.M. 1999. Pseudo-nitzschia species (Bacillariophyceae) in
Louisiana coastal waters: Molecular probe field trials, genetic variability, and domoic
acid analyses. J. Phycol. 35, 1368–1378.
85. Dortch, Q., Robichaux, R., Pool, S., Milsted, D., Mire, G., Rabalais, N.N., Soniat, T.M.,
Fryxell, G.A., Turner, R.E. and Parsons, M.L. 1997. Abundance and vertical flux of
Pseudo-nitzschia in the northern Gulf of Mexico. Mar. Ecol. Prog. Ser. 146, 249–
264.
86. Rabalais, N.N., Turner, R.E., Justić, D., Dortch, Q., Wiseman, Jr. W.J. and Sen Gupta,
B.K. 1996. Nutrient changes in the Mississippi River and system responses on the ad-
jacent continental shelf. Estuaries 19, 386–407.
87. Parsons, M.L., Dortch, Q. and Turner, R.E. 2002. Sedimentological evidence of an
increase of Pseudo-nitzschia (Bacillariophyceae) abundance in response to coastal
eutrophication. Limnol. Oceanogr. 47, 551–558.
88. Rabalais, N.N. 2001. Press release, July 26, 2001, Louisiana Universities Marine Con-
sortium, Chauvin, Louisiana (www.lumcon.edu).
89. Dauer, D.M., Rodi, Jr. A.J. and Ranasinghe, J.A. 1992. Effects of low dissolved oxy-
gen events on the macrobenthos of the lower Chesapeake Bay. Estuaries 15, 384–
391.
90. Rosenberg, R. 1990. Negative oxygen trends in Swedish coastal bottom waters. Mar.
Pollut. Bull.21, 335–339.
91. Meyer-Reil, L.-A. and Köster, M. 2000. Eutrophication of marine waters: effects on
benthic microbial communities. Mar. Pollut. Bull. 41, 255–263.
92. Boesch, D.F., Brinsfield, R.B. and R.E. Magnien. 2001. Chesapeake Bay
eutrophication: Scientific understanding, ecosystem restoration, and challenges for ag-
riculture. J. Environ. Qual. 30, 303–320.
93. Knowlton, N. 2001. The future of coral reefs. Proc. Natl Acad. Sci., USA 98, 5419–
5425.
94. Smith, S.V. 1981. Responses of Kaneohe Bay, Hawaii, to relaxation of sewage stress.
In: Estuaries and Nutrients. Neilson, B.J. and Cronin, L.E. (eds). Humana Press, Inc.,
Clifton, New Jersey, pp. 391–410.
95. Naim, O. 1993. Seasonal responses of a fringing reef community to eutrophication
(Reunion Island, western Indian Ocean). Mar. Ecol. Prog. Ser. 99, 137–151.
96. LaPointe, B.E. 1997. Nutrient thresholds for eutrophication and macroalgal blooms
on coral reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42, 1119–1131.
97. Stimson, J., Larned, S.T. and Conklin, E. 2001. Effects of herbivory, nutrient levels,
and introduced algae on the distribution and abundance of the invasive macroalga
Disctyosphaeria cavernosa in Kaneohe Bay, Hawaii. Coral Reefs 19. 343–357.
98. Koop, K., Booth, D., Broadbent, A., Brodie, J., Bucher, D., Capone, D., Coll, J.,
Dennison, W., Erdmann, M., Harrison, P., Hoegh-Guldberg, O., Hutchings, P., Jones,
G.B., Larkum, A.W.D., O’Neil, J., Steven, A., Tentor, E., Ward, S., Williamson, J.
and Yellowlees, D. 2001. ENCORE: The effects of nutrient enrichment on coral reefs.
Synthesis of results and conclusions. Mar. Pollut. Bull. 42, 91–120.
99. Szmant, A.M. 2002. Nutrient enrichment on coral reefs: Is it a major cause of coral
reef decline? Estuaries. (In print).
100. Paerl, H.W., Willey, J.D., Go, M., Peierls, B.L., Pinckney, J.L. and Fogel, M.L. 1999.
Rainfall stimulation of primary production in western Atlantic Ocean waters: roles of
different nitrogen sources and co-limiting nutrients. Mar. Ecol. Prog. Ser. 176, 205–
214.
101. Berman-Frank, I., Cullen, J.T., Shaked, Y., Sherrell, R.M. and Falkowski, P.G. 2001.
Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol.
Oceanogr. 46, 1249–1260.
102. Lenes, J.M., Darrow, B.P., Cattrall, C., Heil, C.A., Callahan, M., Vargo, G.A., Byrne,
R.H., Prospero, J.M., Bates, D.E., Fanning, K.A. and Walsh, J.J. 2001. Iron fertiliza-
tion and the Trichodesmium response on the West Florida shelf. Limnol. Oceanogr.
46, 1261–1277.
103. Downing, J.A., McClain, M., Twilley, R., Melack, J.M., Elser, J., Rabalais, N.N.,
Lewis, Jr. W.M., Turner, R.E., Corredor, R., Soto, D., Yanez-Arancibia, A., Kopaska,
J.A. and Howarth, R.R. 1999. The impact of accelerating land-use change on the N-
cycle of tropical ecosystems: current conditions and projected changes. Biogeochem.
46, 109–148.
104. Grimvall, A., Stålnacke, P. and Tonderski, A. 2000. Time scales of nutrient losses
from land to sea-a European perspective. Ecol. Engineering 14, 363–371.
105. Boesch, D.F. 2001. Science and integrated drainage basin coastal management.
Chesapeake Bay and Mississippi Delta. In: Science and Integrated Coastal Manage-
ment. von Bodungen, B. and Turner, R.K. (eds). Dahlem University Press, Berlin, pp.
37–50.
106. Li, Y. and Zhang, J. 1999. Agricultural diffuse pollution from fertilizers and pesti-
cides in China. Water Sci. Technol. 39, 25–32.
107. I thank the US National Oceanic and Atmospheric Administration, Coastal Ocean Pro-
gram, for research funds that supported this synthesis, Gene Turner and three anony-
mous referees for helpful comments on the draft manuscript, and Ben Cole for assist-
ance 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
Ambio Vol. 31 No. 2, March 2002