559
Ecological Applications,
8(3), 1998, pp. 559–568
q
1998 by the Ecological Society of America
NONPOINT POLLUTION OF SURFACE WATERS WITH
PHOSPHORUS AND NITROGEN
S. R. C
ARPENTER
,
1
N. F. C
ARACO
,
2
D. L. C
ORRELL
,
3
R. W. H
OWARTH
,
4
A. N. S
HARPLEY
,
5
AND
V. H . S
MITH
6
1
Center for Limnology, 680 North Park Street, University of Wisconsin, Madison, Wisconsin 53706 USA
2
Institute of Ecosystem Studies, Box AB Route 44A, Millbrook, New York 12545 USA
3
Smithsonian Environmental Research Center, P.O. Box 28, Edgewater Maryland 21037 USA
4
Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853 USA
5
USDA-ARS, Pasture Systems and Watershed Management Research Laboratory, Curtin Road,
University Park, Pennsylvania 16802 USA
6
Department of Systematics and Ecology, 6007 Haworth Hall, University of Kansas, Lawrence, Kansas 66045 USA
Abstract.
Agriculture and urban activities are major sources of phosphorus and nitro-
gen to aquatic ecosystems. Atmospheric deposition further contributes as a source of N.
These nonpoint inputs of nutrients are difficult to measure and regulate because they derive
from activities dispersed over wide areas of land and are variable in time due to effects of
weather. In aquatic ecosystems, these nutrients cause diverse problems such as toxic algal
blooms, loss of oxygen, fish kills, loss of biodiversity (including species important for
commerce and recreation), loss of aquatic plant beds and coral reefs, and other problems.
Nutrient enrichment seriously degrades aquatic ecosystems and impairs the use of water
for drinking, industry, agriculture, recreation, and other purposes.
Based on our review of the scientific literature, we are certain that (1) eutrophication
is a widespread problem in rivers, lakes, estuaries, and coastal oceans, caused by over-
enrichment with P and N; (2) nonpoint pollution, a major source of P and N to surface
waters of the United States, results primarily from agriculture and urban activity, including
industry; (3) inputs of P and N to agriculture in the form of fertilizers exceed outputs in
produce in the United States and many other nations; (4) nutrient flows to aquatic ecosystems
are directly related to animal stocking densities, and under high livestock densities, manure
production exceeds the needs of crops to which the manure is applied; (5) excess fertilization
and manure production cause a P surplus to accumulate in soil, some of which is transported
to aquatic ecosystems; and (6) excess fertilization and manure production on agricultural
lands create surplus N, which is mobile in many soils and often leaches to downstream
aquatic ecosystems, and which can also volatilize to the atmosphere, redepositing elsewhere
and eventually reaching aquatic ecosystems.
If current practices continue, nonpoint pollution of surface waters is virtually certain
to increase in the future. Such an outcome is not inevitable, however, because a number
of technologies, land use practices, and conservation measures are capable of decreasing
the flow of nonpoint P and N into surface waters.
From our review of the available scientific information, we are confident that: (1)
nonpoint pollution of surface waters with P and N could be reduced by reducing surplus
nutrient flows in agricultural systems and processes, reducing agricultural and urban runoff
by diverse methods, and reducing N emissions from fossil fuel burning; and (2) eutrophi-
cation can be reversed by decreasing input rates of P and N to aquatic ecosystems, but
rates of recovery are highly variable among water bodies. Often, the eutrophic state is
persistent, and recovery is slow.
Key words: agriculture; estuary; eutrophication; lake; nitrogen; nonpoint pollution; phosphorus;
river; runoff; stream.
Manuscript received 15 December 1997; accepted 15 January 1998. Reprints of this 10-page report are available for $1.50
each. Prepayment is required. Order reprints from the Ecological Society of America. Attention: Reprint Department, 2010
Massachusetts Avenue, NW, Suite 400, Washington, D.C. 20036.
560 S. R. CARPENTER ET AL.
Ecology
Vol. 8, No. 3
T
ABLE
1. Characteristics of point and nonpoint sources of
chemical inputs to receiving waters recognized by statutes
of the United States (modified from Novotny and Olem
1994).
Point sources
Wastewater effluent (municipal and industrial)
Runoff and leachate from waste disposal sites
Runoff and infiltration from animal feedlots
Runoff from mines, oil fields, unsewered industrial sites
Storm sewer outfalls from cities with a population
.
100000
Overflows of combined storm and sanitary sewers
Runoff from construction sites
.
2ha
Nonpoint sources
Runoff from agriculture (including return flow from irri-
gated agriculture)
Runoff from pasture and range
Urban runoff from unsewered areas and sewered areas with
a population
,
100 000
Septic tank leachate and runoff from failed septic systems
Runoff from construction sites
,
2ha
Runoff from abandoned mines
Atmospheric deposition over a water surface
Activities on land that generate contaminants, such as log-
ging, wetland conversion, construction, and development
of land or waterways
I
NTRODUCTION
People are attracted to lakes, rivers, and coastlines
for diverse reasons. Clean water is a crucial resource
for drinking, irrigation, industry, transportation, rec-
reation, fishing, hunting, support of biodiversity, and
sheer esthetic enjoyment. Throughout human history,
water has been used to wash away and dilute pollutants.
Pollutant inputs have increased in recent decades and
have degraded water quality of many rivers, lakes, and
coastal oceans. Degradation of these vital water re-
sources can be measured as the loss of natural systems,
their component species, and the amenities that they
provide (U.S. EPA 1996, Postel and Carpenter 1997).
Water shortages are increasingly common and likely to
become more severe in the future (Postel et al. 1996,
Postel 1997). Water shortage and poor water quality
are linked, because contamination reduces the supply
of water and increases the costs of treating water for
use. Preventing pollution is among the most cost-ef-
fective means of increasing water supplies.
Eutrophication caused by excessive inputs of phos-
phorus (P) and nitrogen (N) is the most common im-
pairment of surface waters in the United States (U.S.
EPA 1990), with impairment measured as the area of
surface water not suitable for designated uses such as
drinking, irrigation, industry, recreation, or fishing. Eu-
trophication accounts for
;
50% of the impaired lake
area and 60% of the impaired river reaches in the Unit-
ed States (U.S. EPA 1996), and is the most widespread
pollution problem of U.S. estuaries (NRC 1993
a
). Oth-
er important causes of surface-water degradation are
siltation caused by erosion from agriculture, logging
and construction (which also contribute to eutrophi-
cation), acidification from atmospheric sources and
mine drainage, contamination by toxins, introduction
of exotic species, and hydrologic changes (NRC 1992).
Chemical inputs to rivers, lakes, and oceans are clas-
sified as
point
or
nonpoint
sources (Table 1). Pollutant
discharges from point sources such as municipal sew-
age treatment plants tend to be continuous, with little
variability over time. Often they can be monitored by
measuring discharge and chemical concentrations pe-
riodically at a single place. Consequently, point sources
are relatively simple to measure and regulate, and can
often be controlled by treatment at the source. Nonpoint
inputs can also be continuous, but are more often in-
termittent and linked to seasonal agricultural activity
or irregular events, such as heavy precipitation or major
construction. Nonpoint inputs often derive from exten-
sive areas of land and are transported overland, un-
derground, or through the atmosphere to receiving wa-
ters. Consequently, nonpoint sources are difficult to
measure and regulate. Control of nonpoint pollution
centers on land management practices and control of
release of pollutants to the atmosphere, and may affect
the daily activities of millions of people.
Nonpoint inputs are the major source of water pol-
lution in the United States (U.S. EPA 1990, 1996). The
National Water Quality Inventory stated that ‘‘the more
we look, the more we find’’ (U.S. EPA 1988). For ex-
ample, 72–82% of eutrophic lakes would require con-
trol of nonpoint phosphorus inputs to meet water qual-
ity standards, even if point inputs were reduced to zero
(Gakstatter et al. 1978).
In many cases, point sources of water pollution have
been reduced, owing to their relative ease of identifi-
cation and control. Point sources are still substantial
in some parts of the world, and may increase with future
expansion of urban areas and aquaculture. This report
focuses on nonpoint sources, not because point sources
are unimportant, but because nonpoint inputs are often
overlooked. In addition, (1) restoration of most eu-
trophic waters requires the reduction of nonpoint inputs
of P and N; (2) we have a sound scientific understand-
ing of the causes of nonpoint nutrient pollution and,
in many cases, we have the technical knowledge needed
to decrease nonpoint pollution to levels compatible
with water quality standards; and (3) the most impor-
tant barriers to control of nonpoint nutrient pollution
appear to be social, political, and institutional. We hope
that our summary of the scientific basis of the problem
will inform and support the debate about solutions.
W
HY
I
S
N
ONPOINT
P
AND
NP
OLLUTION A
C
ONCERN
?
Eutrophication
Scope and causes.
—Eutrophication, caused by ex-
cessive inputs of P and N, is a common and growing
problem in lakes, rivers, estuaries, and coastal oceans
(Smith 1998). Freshwater eutrophication has been a
growing problem for decades (OECD 1982, NRC
1992). Both P and N supplies contribute to freshwater
August 1998 561
NONPOINT WATER POLLUTION
T
ABLE
2. Adverse effects on lakes, reservoirs, rivers, and
coastal oceans caused by eutrophication (modified from
Smith 1998).
Increased biomass of phytoplankton
Shifts in phytoplankton to bloom-forming species that may
be toxic or inedible
Increases in blooms of gelatinous zooplankton (in marine
environments)
Increased biomass of benthic and epiphytic algae
Changes in macrophyte species composition and biomass
Death of coral reefs and loss of coral reef communities
Decreases in water transparency
Taste, odor, and water treatment problems
Oxygen depletion
Increased incidence of fish kills
Loss of desirable fish species
Reductions in harvestable fish and shellfish
Decreases in perceived esthetic value of the water body
T
ABLE
3. Nitrogen and phosphorus discharges to surface
waters (in 10
3
Mg/yr) from nonpoint and point sources in
the United States.
Source Nitrogen Phosphorus
Nonpoint sources
Croplands
Pastures
Rangelands
Forests
Other rural lands
Other nonpoint sources
Total
3204
292
778
1035
659
695
6663
615
95
242
495
170
68
1658
Total point sources
Total discharge (nonpoint
1
point)
1495
8158
330
2015
Nonpoint as percentage of total 82% 84%
Note:
Data are modified from Havens and Steinman (1995)
and Gianessi et al. (1986).
eutrophication (OECD 1982). For many lakes, exces-
sive P inputs are the primary cause (Schindler 1977).
Eutrophication is also widespread and rapidly ex-
panding in estuaries and coastal seas of the developed
world (NRC 1993
a
, Nixon 1995). For most temperate
estuaries and coastal ecosystems, N is the element most
limiting to primary production and most responsible
for eutrophication (Howarth 1988, NRC 1993
a
, Ho-
warth et al. 1996, Nixon et al. 1996). Although N is
the major factor in eutrophication of most estuaries and
coastal seas, P is also an essential element that con-
tributes to coastal eutrophication. It is, in fact, the dom-
inant control of primary production in some coastal
ecosystems.
Consequences.
—Eutrophication has many negative
effects on aquatic ecosystems (Table 2). Perhaps the
most obvious consequence is the increased growth of
algae and aquatic weeds that interfere with use of the
water for fisheries, recreation, industry, agriculture,
and drinking. Oxygen shortages caused by senescence
and decomposition of nuisance plants cause fish kills.
Eutrophication causes the loss of habitats, including
aquatic plant beds in fresh and marine waters and coral
reefs of tropical coasts (NRC 1993
a
, Jeppesen et al.
1998). Eutrophication is a factor in the loss of aquatic
biodiversity (Seehausen et al. 1997).
Explosive growths of nuisance algae are among the
most pernicious effects of eutrophication (Anderson
and Garrison 1997). These algae are harmful to live-
stock, humans, and other organisms. In marine eco-
systems, algal blooms (red or brown tides) cause wide-
spread problems by releasing toxins and by causing
anoxia when oxygen is consumed as dead algae de-
compose. The incidence of harmful algal blooms in
coastal oceans has increased in recent years (Hallegraef
1993). The increase is linked to coastal eutrophication
and other factors, such as changes in marine food webs
that may reduce grazing or increase nutrient recycling.
The blooms have severe negative impacts on aquacul-
ture and shellfisheries (Shumway 1990). They cause
shellfish poisoning in humans and have caused signif-
icant mortality in marine mammals (Anderson 1994).
A newly discovered toxic dinoflagellate has been as-
sociated with mortality of finfish on the U.S. Atlantic
coast (Burkholder et al. 1992). The highly toxic, vol-
atile chemical produced by this alga can cause long-
term neurological damage to people who come in con-
tact with it.
In freshwater, blooms of cyanobacteria (blue-green
algae) are a prominent symptom of eutrophication (Ko-
tak et al. 1993, McComb and Davis 1993, Smith 1998).
These blooms contribute to a wide range of water-re-
lated problems including summer fish kills, foul odors,
unpalatability of drinking water, and formation of tri-
halomethane during water chlorination in treatment
plants (Palmstrom et al. 1988, Kotak et al. 1994). Wa-
ter-soluble neuro- and hepatotoxins, released when cy-
anobacterial blooms die or are ingested, can kill live-
stock and may pose a serious health hazard to humans
(Lawton and Codd 1991, Martin and Cooke 1994).
Contribution of nonpoint pollution.
—Nonpoint
sources are now the dominant inputs of P and N to
most U.S. surface waters (Table 3). Nonpoint inputs of
P cause eutrophication of a large area of lakes and
reservoirs in the United States (U.S. EPA 1990, 1996,
NRC 1992). Nonpoint sources are also the dominant
source of P and N to most reaches of U.S. rivers (New-
man 1995), but point sources still contribute
.
50% of
the P and N reaching rivers from urbanized areas. Non-
point N sources are responsible for
.
90% of the N
inputs to over one-half of the 86 rivers studied. Non-
point P sources contributed
.
90% of the P in one-third
of these rivers (Newman 1995).
For many estuaries and coastal seas, nonpoint
sources are the dominant N inputs (Nixon and Pilson
1983, NRC 1993
a
). Considering the entire coastline of
the North Atlantic Ocean, nonpoint sources of N are
;
ninefold greater than are inputs from wastewater
treatment plants (Howarth et al. 1996). In some coastal
areas, however, N inputs come primarily from waste-
water treatment plants. Although nonpoint inputs of P
are often significant, point source inputs of P are high
562 S. R. CARPENTER ET AL.
Ecology
Vol. 8, No. 3
F
IG
. 1. Inputs, outputs, and processes of transport of P and N from agricultural land.
in many marine environments (van der Leeden et al.
1990).
Remediation.
—Reversal of eutrophication requires
the reduction of P and N inputs (NRC 1992). Recovery
can sometimes be accelerated by combining input con-
trols with other management methods (Sas 1989, NRC
1992, Cooke et al. 1993). Active intervention may be
necessary, because the eutrophic state is relatively sta-
ble in lakes (Jeppesen et al. 1991, NRC 1992, Carpenter
and Cottingham 1997). Some mechanisms that stabilize
eutrophic conditions are effective internal recycling of
P, loss of rooted aquatic plants leading to destabiliza-
tion of sediments, and changes in the food web that
reduce grazing of nuisance algae (Carpenter and Cot-
tingham 1997). Less is known about the stability of
eutrophication in estuaries and coastal oceans, but the
eutrophic state may be less stable because nutrients
may be diluted and flushed away rapidly in open, well-
mixed coastal oceans. However, in relatively confined,
shallow marine waters such as the Baltic Sea, nutrients
may be trapped and eutrophication may be as persistent
as it is in lakes (Jansson 1995).
Direct health effects
Phosphorus in water is not considered to be directly
toxic to humans and animals (Amdur et al. 1991). Be-
cause of this, no drinking water standards have been
established for P (U.S. EPA 1990). Any toxicity caused
by P in freshwaters is indirect. The proximal cause is
toxic algal blooms or anoxic conditions stimulated by
P pollution.
Nitrate pollution, in contrast, poses a direct health
threat to humans and other mammals. NO
3
in water is
toxic at high concentrations and has been linked to
methemoglobinemia in infants and toxic effects on
livestock (Sandstedt 1990, Amdur et al. 1991). The
EPA has established a maximum contaminant level for
NO
3
-N in drinking water of 10 mg/L (45 mg NO
3
/L)
to protect babies under 3–6 mo of age. This age group
is most sensitive because bacteria that live in an infant’s
digestive tract can reduce NO
3
to nitrite, causing con-
version of hemoglobin into methemoglobin, which in-
terferes with the oxygen-carrying ability of blood (Am-
dur et al. 1991). Nitrate can also be toxic to livestock
if reduced to nitrite, which causes methemoglobinemia
and abortions in cattle. NO
3
-N levels of 40–100 mg/L
in drinking water are considered risky unless the feed
is low in NO
3
and fortified with vitamin A (Sandstedt
1990).
W
HAT
A
RE THE
S
OURCES OF
N
ONPOINT
P
OLLUTION
?
Nonpoint P and N pollution is caused primarily by
agricultural and urban activities (Novotny and Olem
1994, Sharpley et al. 1994). Atmospheric deposition
from diverse sources can add significant amounts of N
to surface waters (Howarth et al. 1996). Agriculture is
the predominant source of nonpoint nutrient pollution
in the United States (NRC 1992, U.S. EPA 1996).
Agriculture
On the world’s agricultural lands, nutrient transport
by farming systems has overwhelmed natural nutrient
cycles (Fig. 1). Globally, more nutrients are added as
fertilizers than are removed as produce. Fertilizers are
moved from areas of manufacture to areas of crop pro-
duction. They are partly incorporated into crops, which
are then moved to localized areas of human consump-
tion and livestock production. Thus, there is a net trans-
port of P and N from sites of fertilizer manufacture to
sites of fertilizer deposition and manure production
(Beaton et al. 1995). This flux creates a nutrient surplus
on agricultural lands, the underlying cause of nonpoint
pollution from agriculture.
Fertilizer.
—Phosphorus is accumulating in the
world’s agricultural soils. Between 1950 and 1995,
;
600
3
10
6
Mg of fertilizer P were applied to Earth’s
August 1998 563
NONPOINT WATER POLLUTION
T
ABLE
4. Phosphorus balance and efficiency of plant and animal uptake of P for the United States (N.R.C. 1993
b
) and
several European countries (Isermann 1991).
Nation
Area in
agriculture
(10
6
ha)
P input
(kg·ha
2
1
·yr
2
1
)
Fertilizer Feed
P output
(kg·ha
2
1
·yr
2
1
)
Animal Plant
P surplus
(kg·ha
2
1
·yr
2
1
)
Efficiency of uptake (%)
Plant Animal Total
East Germany
West Germany
Ireland
Netherlands
Switzerland
United Kingdom
United States
6.2
12.0
5.7
2.3
1.1
18.5
394.7
25
27
11
18
22
9
39
6
10
1
44
11
3
5
3
10
3
17
6
2
13
1
3
1
5
4
1
5
27
24
8
40
23
9
26
59
76
72
69
91
55
56
10
34
22
24
18
18
15
11
35
30
38
28
25
33
surface, primarily on croplands (Brown et al. 1997,
FAO 1950–1995). During the same time period,
;
250
3
10
6
Mg of P were removed from croplands through
harvest (Beaton et al. 1995, Brown et al. 1997, FAO
1950–1995). Some of the harvested P (
;
50
3
10
6
Mg)
was reapplied to cropland as animal manure (NRC
1993
b
). Thus, the net addition of P to croplands over
this period was
;
400
3
10
6
Mg. This applied P may
either remain in soils or be exported to surface waters
by erosion or leaching. The majority of applied P re-
mains on croplands, with only 3–20% leaving by export
to surface waters (Caraco 1995). It is likely, therefore,
that
;
350
3
10
6
Mg of P have accumulated in the
world’s croplands. The standing stock of P in the upper
10 cm of soil in the world’s croplands is
;
1300 Mg
(Pierrou 1975). Therefore, the net addition of 350
3
10
6
Mg between 1950 and 1995 would have increased
the P content of agricultural soils by
;
25%. In the
United States and Europe, only
;
30% of the P input
in fertilizers is output in produce, resulting in an av-
erage accumulation rate of 22 kg·ha
2
1
·y
2
1
for surplus
P (Table 4). At the watershed scale, excess inputs of
P to agriculture relative to outputs in produce are close-
ly linked to eutrophication of surface waters (Fluck et
al. 1992).
Global industrial N fixation for fertilizers has in-
creased steeply from nearly zero in the 1940s to
;
80
3
10
6
Mg/yr (Vitousek et al. 1997). In the United States
and Europe, only 18% of the N input in fertilizer is
removed from farms in produce, leaving behind, on
average, 174 kg·ha
2
1
·y
2
1
of surplus N (Isermann 1991,
NRC 1993
b
). This surplus may accumulate in soils,
erode or leach to surface and ground waters, or enter
the atmosphere (Vitousek et al. 1997). N is added to
the atmosphere through volatilization of NH
3
(Schle-
singer and Hartley 1992) and microbial generation of
N
2
O (Eichner 1990). N
2
O is a gas that contributes to
global warming and can catalyze the destruction of
ozone (Vitousek et al. 1997). Much of the N volatilized
to the atmosphere is redeposited on land or water and
eventually enters aquatic ecosystems (Howarth et al.
1996).
Manure.
—Intensive animal production generally in-
volves feeding large numbers of animals in small areas
(NRC 1993
b
). For example, only 4% of the cattle feed-
lots in the United States produce 84% of the cattle
(NRC 1993
b
). These large concentrations of animals
create enormous amounts of waste. Disposal problems
are comparable to those for raw human sewage, but the
regulatory standards for animal waste are generally far
less stringent than those for human sewage.
Nutrients in manure can be recycled by applying the
manure to cropland. However, manure yields from con-
centrated livestock operations often exceed the capac-
ity of croplands to sequester the nutrients (NRC
1993
b
). At typical stocking rates for feedlots, an area
of cropland
;
1000 times greater than the feedlot area
is required to distribute manure nutrients at levels sim-
ilar to crop demand (NRC 1993
b
). This much land may
not be available, so manure is applied to excess. These
nutrients build up in soil, run off or infiltrate to water
supplies, or (in the case of N) can enter the atmosphere.
Transport to aquatic ecosystems.
—Increased fluxes
of P and N to surface waters have been measured after
application of fertilizer or manure to farm land (Sharp-
ley and Rekolainen 1996). Fertilizer P and N losses in
runoff are generally
,
5% of that applied. Manurial
losses can be slightly higher (up to 20%, if rainfall
immediately follows application). These percentages
underestimate the total N flux to aquatic ecosystems
because they do not include infiltration and leaching,
which ultimately carry N to ground and surface waters.
N export from agricultural ecosystems to water, as a
percentage of fertilizer inputs, ranges from 10% to 40%
for loam and clay soils to 25% to 80% for sandy soils
(Howarth et al. 1996). In general, flux rates of nutrients
to water from fertilizer and manure are influenced by
the rate, season, chemical form, and method of nutrient
application; amount and timing of rainfall after appli-
cation; and vegetative cover. The greater proportional
losses of P and N from manure may result from higher
P and N application rates and less flexibility in the
timing of applications (Sharpley and Rekolainen 1996).
The amount of P lost to surface waters increases with
the P content of the soil (Fig. 2). Relationships similar
to those in Fig. 2 have been demonstrated for a diversity
of soils (Sharpley et al. 1996). Fig. 2 shows losses of
dissolved P, but even more P is transported as particles.
