Nutrient Limitation of Net Primary Production in Marine Ecosystems
01 Jan 1988-Annual Review of Ecology, Evolution, and Systematics (Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303-0139, USA)-Vol. 19, Iss: 1, pp 89-110
TL;DR: There is a feeling among many limnologists and environmental engineers who study lakes that marine ecosystems also probably are phosphorus limited, and environmental management agencies often assume that phosphorus limitation in marine ecosystems is the rule.
Abstract: The question of nutrient limitation of primary production in estuaries and other marine ecosystems has engendered a great deal of debate. Although nitrogen is often named as the primary limiting nutrient in seawater (3, 17-19, 50, 52, 55, 61, 76, 80), this is by no means universally accepted. Many workers have argued that phosphorus is limiting (58, 71), that both nitrogen and phosphorus can simultaneously be limiting (9), or that primary production can switch seasonally from being nitrogen-limited to phosphorus-limited (6, 46). Others argue that nutrients are not limiting at all in many marine ecosystems, including highly oligotrophic waters (15). To some extent these disagreements result from poor communication due to different definitions of nutrient limitation. Considerable argument also occurs over the various methods and approaches used to estimate nutrient limitation. Limnologists in particular have tended to be critical of the methods often used to study nutrient limitation in marine ecosystems (23). Nutrient limitation in lakes has historically received more study than that in estuaries, and most mesotrophic and eutrophic north-temperate lakes are phosphorus limited (8, 62, 63, 66, 81). Thus, there is a feeling among many limnologists and environmental engineers who study lakes that marine ecosystems also probably are phosphorus limited. Lacking strong mechanistic arguments to explain why nutrient limitation might be different in estuaries than in lakes, environmental management agencies often assume that phosphorus limitation in marine ecosystems is the rule.
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TL;DR: In this article, a review of available scientific evidence shows that human alterations of the nitrogen cycle have approximately doubled the rate of nitrogen input into the terrestrial nitrogen cycle, with these rates still increasing; increased concentrations of the potent greenhouse gas N 2O globally, and increased concentration of other oxides of nitrogen that drive the formation of photochemical smog over large regions of Earth.
Abstract: Nitrogen is a key element controlling the species composition, diversity, dynamics, and functioning of many terrestrial, freshwater, and marine ecosystems. Many of the original plant species living in these ecosystems are adapted to, and function optimally in, soils and solutions with low levels of available nitrogen. The growth and dynamics of herbivore populations, and ultimately those of their predators, also are affected by N. Agriculture, combustion of fossil fuels, and other human activities have altered the global cycle of N substantially, generally increasing both the availability and the mobility of N over large regions of Earth. The mobility of N means that while most deliberate applications of N occur locally, their influence spreads regionally and even globally. Moreover, many of the mobile forms of N themselves have environmental consequences. Although most nitrogen inputs serve human needs such as agricultural production, their environmental conse- quences are serious and long term. Based on our review of available scientific evidence, we are certain that human alterations of the nitrogen cycle have: 1) approximately doubled the rate of nitrogen input into the terrestrial nitrogen cycle, with these rates still increasing; 2) increased concentrations of the potent greenhouse gas N 2O globally, and increased concentrations of other oxides of nitrogen that drive the formation of photochemical smog over large regions of Earth; 3) caused losses of soil nutrients, such as calcium and potassium, that are essential for the long-term maintenance of soil fertility; 4) contributed substantially to the acidification of soils, streams, and lakes in several regions; and 5) greatly increased the transfer of nitrogen through rivers to estuaries and coastal oceans. In addition, based on our review of available scientific evidence we are confident that human alterations of the nitrogen cycle have: 6) increased the quantity of organic carbon stored within terrestrial ecosystems; 7) accelerated losses of biological diversity, especially losses of plants adapted to efficient use of nitrogen, and losses of the animals and microorganisms that depend on them; and 8) caused changes in the composition and functioning of estuarine and nearshore ecosystems, and contributed to long-term declines in coastal marine fisheries.
5,729 citations
Cites background from "Nutrient Limitation of Net Primary ..."
...…seas The eutrophication of estuaries and coastal seas is one of the best-documented and best-understood consequences of human-altered N cycling (Howarth 1988, NRC 1993, Justic et al. 1995, Nixon 1995, Nixon et al. 1996); it represents perhaps the greatest threat to the integrity of coastal…...
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TL;DR: In this article, a review of the available scientific information, they are confident that 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, but rates of recovery are highly variable among water bodies.
Abstract: Agriculture and urban activities are major sources of phosphorus and nitrogen 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 overenrichment 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) eutrophication 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.
5,662 citations
Cites background from "Nutrient Limitation of Net Primary ..."
...For most temperate estuaries and coastal ecosystems, N is the element most limiting to primary production and most responsible for eutrophication (Howarth 1988, NRC 1993a, Howarth et al. 1996, Nixon et al. 1996)....
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TL;DR: A large-scale meta-analysis of experimental enrichments shows that P limitation is equally strong across these major habitats and that N and P limitation are equivalent within both terrestrial and freshwater systems.
Abstract: The cycles of the key nutrient elements nitrogen (N) and phosphorus (P) have been massively altered by anthropogenic activities. Thus, it is essential to understand how photosynthetic production across diverse ecosystems is, or is not, limited by N and P. Via a large-scale meta-analysis of experimental enrichments, we show that P limitation is equally strong across these major habitats and that N and P limitation are equivalent within both terrestrial and freshwater systems. Furthermore, simultaneous N and P enrichment produces strongly positive synergistic responses in all three environments. Thus, contrary to some prevailing paradigms, freshwater, marine and terrestrial ecosystems are surprisingly similar in terms of N and P limitation.
3,543 citations
Cites background from "Nutrient Limitation of Net Primary ..."
...In coastal marine systems, nitrogen has historically been considered to be the predominant limiting nutrient (Howarth 1988)....
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...In coastal marine systems, nitrogen has historically been considered to be the predominant limiting nutrient ( Howarth 1988 )....
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TL;DR: In this paper, the authors examine both how the biogeochemistry of the nitrogen cycle could cause limitation to develop, and how nitrogen limitation could persist as a consequence of processes that prevent or reduce nitrogen fixation.
Abstract: The widespread occurrence of nitrogen limitation to net primary production in terrestrial and marine ecosystems is something of a puzzle; it would seem that nitrogen fixers should have a substantial competitive advantage wherever nitrogen is limiting, and that their activity in turn should reverse limitation. Nevertheless, there is substantial evidence that nitrogen limits net primary production much of the time in most terrestrial biomes and many marine ecosystems. We examine both how the biogeochemistry of the nitrogen cycle could cause limitation to develop, and how nitrogen limitation could persist as a consequence of processes that prevent or reduce nitrogen fixation. Biogeochemical mechansism that favor nitrogen limitation include: A number of mechanisms could keep nitrogen fixation from reversing nitrogen limitation. These include: The possible importance of these and other processes is discussed for a wide range of terrestrial, freshwater, and marine ecosystems.
3,332 citations
TL;DR: Two brief case studies demonstrate that nutrient loading restriction is the essential cornerstone of aquatic eutrophication control, and results of a preliminary statistical analysis are presented consistent with the hypothesis that anthropogenic emissions of oxidized nitrogen could be influencing atmospheric levels of carbon dioxide via nitrogen stimulation of global primary production.
2,702 citations
Cites background from "Nutrient Limitation of Net Primary ..."
...The supply rate of N and P also strongly in¯uences the growth of algae and vascular plants in freshwater and marine ecosystems (Vollenweider, 1968; Hecky and Kilham, 1988; Howarth, 1988; Smith, 1998)....
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...These trends in anthropogenic N inputs are of great concern because nutrient limitation of algal production has been demonstrated or inferred in many estuarine and marine waters (Hecky and Kilham, 1988; Howarth, 1988, 1993; Vitousek and Howarth, 1991; Lapointe and Clark 1992; Downing, 1997)....
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...The supply rate of N and P also strongly in ̄uences the growth of algae and vascular plants in freshwater and marine ecosystems (Vollenweider, 1968; Hecky and Kilham, 1988; Howarth, 1988; Smith, 1998)....
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References
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Journal Article•
3,481 citations
2,515 citations
TL;DR: The primary production in the oceans results from allochthonous nutrient inputs to the euphotic zone (new production) and from nutrient recycling in the surface waters (regenerated production) as discussed by the authors.
Abstract: Primary production in the oceans results from allochthonous nutrient inputs to the euphotic zone (new production) and from nutrient recycling in the surface waters (regenerated production). Global new production is of the order of 3.4−4.7 × 109 tons of carbon per year and approximates the sinking flux of paniculate organic matter to the deep ocean.
2,439 citations
TL;DR: Removal of phosphate from detergents is not likely to slow the eutrophication of coastal marine waters, and its replacement with nitrogen-containing nitrilotriacetic acid may worsen the situation.
Abstract: The distribution of inorganic nitrogen and phosphorus and bioassay experiments both show that nitrogen is the critical limiting factor to algal growth and eutrophication in coastal marine waters. About twice the amount of phosphate as can be used by the algae is normally present. This surplus results from the low nitrogen to phosphorus ratio in terrigenous contributions, including human waste, and from the fact that phosphorus regenerates more quickly than ammonia from decomposing organic matter. Removal of phosphate from detergents is therefore not likely to slow the eutrophication of coastal marine waters, and its replacement with nitrogen-containing nitrilotriacetic acid may worsen the situation.
1,828 citations
TL;DR: It is concluded that the extent and severity of N limitation in the marine environment remain an open question, despite the fact that by the late seventies the evidence for P limitation had become so great that phosphorus control was recommended as the legislated basis for controlling eutrophication in North American and European inland waters.
Abstract: Phytoplankton can become limited by the availability of nutrients when light and temperature are adequate and loss rates are not excessive. The current paradigms for nutrient limitations in freshwater, estuarine, and marine environments are quite different. A review of the experimental and observational data used to infer P or N limitation of phytoplankton growth indicates that P limitation in freshwater environments can be demonstrated rigorously at several hierarchical levels of system complexity, from algal cultures to whole lakes. A similarly rigorous demonstration of N limitation has not been achieved for marine waters. Therefore, we conclude that the extent and severity of N limitation in the marine environment remain an open question. Culture studies have established that internal cellular concentrations of nutrients determine phytoplankton growth rates, and these studies have shown that it is often difficult to relate growth rates to external concentrations, especially in natural situations. This should lead to a greater reliance on the composition of particulate matter and biomass-based physiological rates to infer nutrient limitation. Such measurements have demonstrated their utility in a wide variety of freshwater and marine environments, and, most importantly, they can be applied to systems that are difficult to manipulate experimentally or budget accurately. Dissolved nutrient concentrations are most useful in determining nutrient loading rates of aquatic ecosystems. The relative proportions of nutrients supplied to phytoplankton can be a strong selective force shaping phytoplankton communities and affecting the biomass yield per unit of limiting nutrient. A current dogma of aquatic science is that marine and estuarine phytoplankton tend to be nitrogen limited, while freshwater phytoplankton tend to be phosphorus limited. Carpenter and Capone (1983) documented the preeminence of N studies in the literature on brackish and marine ecosystems. In 1970 there were equal numbers of references per year to N and P. The decade of the seventies saw a nearly fourfold increase in references to N, while the number of P references per year remained essentially unchanged. No trend was evident for the freshwater literature despite the fact that by the late seventies the evidence for P limitation had become so great that phosphorus control was recommended as the legislated basis for controlling eutrophication in North American and European inland waters (e.g.
1,594 citations