COMMENTARY

Phosphorus control is critical to mitigating

Stephen R. Carpenter* Center for , University of Wisconsin, Madison, WI 53706

he Midwest floods of 2008 added more than just water to the region’s lakes, reservoirs, and rivers. Runoff from farms Tand towns carries a heavy load of silt, nutrients, and other pollutants. The nu- trients trigger blooms of algae, which taint drinking water. Death and decay of the algae depletes oxygen, kills fish and bottom-dwelling animals, and thereby creates ‘‘dead zones’’ in the body of wa- ter. The syndrome of excessive nutrients, noxious algae, foul water, and dead zones—which ecologists call eutrophica- tion—is depressingly familiar to those who depend on water from rich agricul- tural regions. The cure sounds simple: decrease in- puts of nutrients, especially nitrogen (N) and phosphorus (P). But which nutrient, and how deeply should the inputs be cut? In this issue of PNAS, Schindler et al. (1) present a remarkable 37-year ex- periment on nutrient management in Canadian lakes which shows that P in- puts directly control algae blooms. Sur- prisingly, however, the authors also observed that algae blooms are made Fig. 1. Surface blooms of cyanobacteria (Microcystis aeruginosa) in lakes Mendota and Monona, worse if N inputs are decreased without Madison, Wisconsin. Although the lakes can exhibit temporary symptoms of nitrogen limitation during summer blooms (14), eutrophication of these lakes is driven by phosphorus runoff from agricultural and also decreasing P inputs. This finding is urban lands. False-color LandSat image processed to highlight surface bloom. (Image courtesy North of critical importance for current pro- Temperate Lakes Long Term Ecological Research Program, http://lter.limnology.wisc.edu.) grams aimed at mitigating eutrophica- tion of both freshwaters and coastal oceans. and a host of other products. The global ment. Reactive N and P differ greatly in Human activity has greatly increased P flux to the biosphere increased from their mobility in the environment. Reac- the inputs of reactive N and P to the Ϸ10–15 Tg P yearϪ1 in preindustrial tive N is transported rapidly in the at- biosphere. Reactive N (biologically ac- times to 33–39 Tg P yearϪ1 in 2000 (3). mosphere and hydrosphere. For exam- tive forms such as nitrate, ammonia, or Excess P added to cropland accumulates ple, nitrate is highly mobile in groundwater, and ammonia can move organic N compounds, in contrast to N2 in soil, which can be eroded to surface gas, which is not used by organisms ex- water. Global P production appears to far through the atmosphere before en- cept for a few nitrogen-fixing species) is be in decline (http://energybulletin.net/ tering aquatic ecosystems. In contrast, P tends to be bound to soil or sediment supplied by natural sources, as well as node/33164), suggesting that conserva- particles or tightly conserved by organ- by human activities such as industrial N2 tion and recycling of P could help sus- isms. Atmospheric transport of P is lim- fixation, combustion, and planting of tain crop production and reduce ited, and erosion and transport of P in soybeans and other N2-fixing crops. pollution of surface waters. particles can be slow. Differences in Global flux of reactive N to the bio- N and P from farmland runoff or in- mobility, combined with great spatial sphere from food production has in- dustrial and municipal discharges are heterogeneity in abundance, lead to Ϫ creased from Ϸ15 Tg N year 1 in 1860 associated with widespread and expand- considerable variability among ecosys- to Ϸ187 Tg N yearϪ1 in 2005 (2). Addi- ing eutrophication of freshwaters and tems in supply rates of reactive N and P tional reactive N is fixed for industrial coastal zones (4) (Fig. 1). Globally, over (8). Therefore, it is difficult to infer or household use or is inadvertently cre- long time scales of centuries to millen- drivers of eutrophication from global ated as a byproduct of fossil fuel com- nia, P appears to be the nutrient that fluxes alone. bustion. Excess reactive N enters constrains biotic production of freshwa- groundwater, surface water, or the ter and ocean ecosystems (5–7). How- atmosphere. ever, long-term global averages fail to Author contributions: S.R.C. wrote the paper. P enters the biosphere by natural express the enormous heterogeneity of The author declares no conflict of interest. weathering of rock, as well as through reactive N and P supplies to particular See companion article on page 11254. mining and other land disturbances by sites over days to decades—the space *E-mail: [email protected]. humans. Mined P is used in fertilizers and time scales of ecosystem manage- © 2008 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0806112105 PNAS ͉ August 12, 2008 ͉ vol. 105 ͉ no. 32 ͉ 11039–11040 Downloaded by guest on September 27, 2021 Fifty years ago, no one knew for sure blooms. However, the lake remained the floods and nutrient inputs of 2008. what caused eutrophication, even though highly eutrophic, with abundant cyanobac- The has depleted animal pro- the symptoms were well described in teria, even though physiological indicators duction, with severe impacts on fisheries scientific literature. Nutrients were sus- were consistent with N limitation. Blooms for shrimp and finfish. There is wide- pected, but the evidence was not defini- of cyanobacteria are among the most spread agreement that the Gulf of Mexi- tive. Algal abundance was correlated with severe consequences of eutrophication, co’s dead zone could be controlled by re- concentrations of many dissolved com- coating shorelines and boat hulls with ducing flows of nutrients from the two pounds, including N and P. Experiments foul-smelling scum and causing taste and rivers. in closed containers sometimes suggested odor problems in drinking water. In addi- Scientific uncertainty about the effects that inorganic carbon (C) limited eu- tion, some strains are highly toxic. From a of decreased N vs. P inputs may not mat- trophication. Other container experiments water quality perspective, decreasing N ter if management practices control both suggested that N and P were equally limit- inputs alone made eutrophication worse. nutrients at the same time. Control mea- ing for growth of algae and that both It is now generally accepted that P sures for runoff of both N and P include were needed to promote algae blooms. inputs must be decreased to mitigate eu- decreased use of fertilizers, containment Physiological indicators also suggested that trophication of lakes and reservoirs. How- and treatment of manure, tillage practices N and P were about equally limiting to ever, reactive N is often thought to be the that conserve soil, vegetated buffers along algae, except during blooms, when cells key controlling factor for eutrophication shorelines, and maintenance or restoration showed signs of N shortage. The ratio of of estuaries or coastal oceans (9). Evi- of wetlands (13). Croplands sensitive to N to P in the environment, compared dence for N control comes from multiple erosion can be converted to other uses with that in algal cells, often suggested N sources, including N:P ratios, physiological that do not pollute waterways. If human limitation during algae blooms. studies of phytoplankton, cross-ecosystem diets were less rich in meat, fewer fertiliz- The confusion was resolved by a cele- correlations of nutrients and algal produc- ers would be needed to grow grain for brated series of whole-lake experiments tivity, experiments in various-sized con- meat production and less manure would at ’s Experimental Lakes Area tainers (some large and open to the atmo- be produced. These and other practices (7). These experiments showed unequiv- sphere), long-term observations offshore mitigate both N and P release to the envi- ocally that P, and not N or C, caused of sewage treatment plants that have per- ronment. Nonetheless, in some cases it eutrophication. The manipulations pro- turbed N and P somewhat independently may be important to know which nutrient duced massive growth of phytoplankton, over time, and mechanistic arguments is more limiting. Sewage treatment plants, clearly visible in air photos and from about biogeochemical differences in lakes for example, can be engineered to adjust meticulously gathered lake data. Refer- and estuaries (10). The evidence resem- the N:P ratio of discharges to aquatic eco- ence systems enriched with inorganic N bles that from freshwater science in the systems. Information about the relative and C showed no discernible changes. In 1960s, before whole-ecosystem experi- impacts of N and P could be used to de- P-rich lakes, diffusion of inorganic C ments clarified the roles of P and N in sign plants that minimize the cost of eu- from the atmosphere and N2 fixation by eutrophication. Because nearshore marine trophication mitigation. cyanobacteria are sufficient to meet the ecosystems are large, open, and rapidly There are many reasons besides eu- C and N demands of algae blooms. flushed by rivers or currents, it has been trophication to decrease reactive N Thus, evidence of C or N control of impossible to perform massive, whole- pollution of the environment. Reactive eutrophication is an artifact of closed ecosystem experiments with undisturbed N emissions are involved in green- containers and short experimental dura- reference ecosystems. In the absence of house warming, smog, growth of weedy tions. When P is abundant, algae appear such experiments, arguments about the terrestrial plants, and human health to be limited by reactive N, but this roles of N and P in coastal eutrophication impacts from air and groundwater pol- does not mean that N mitigation will are likely to remain unresolved. lution (4). These would be important reduce algae blooms. Nutrient regulation of coastal marine reasons for concern about reactive N Now Schindler et al. (1) present the ecosystems is a critical research topic be- emissions, even if eutrophication was results of a long-term experiment on the cause of the global expansion of dead not considered. mitigation of eutrophication. For 5 years, zones in these environments. By 2005, 146 Yet, the results presented by Schin- a lake was eutrophied by adding excess N coastal marine dead zones had been docu- dler et al. (1) show that a single-minded and P. Then, N inputs were decreased for mented globally, 43 of them in the U.S. focus on control of reactive N would 16 years, so the N:P supply ratio was be- (11). In the northern Gulf of Mexico, nu- have disastrous consequences for low that of algal cells. N fixation by cya- trient discharge from the Mississippi and aquatic resources. To decrease eutrophi- nobacteria made up the N deficit. For the Atchafalaya rivers creates an extensive cation, control of reactive N alone is not final 16 years of the experiment, no N was dead zone during summer (12). The area sufficient—P control is essential and added to the lake and P fertilization con- of this dead zone was Ϸ20,000 km2 in must be included in management pro- tinued. If N can control eutrophication, 2001, roughly the size of New Jersey. It is grams designed to decrease eutrophica- this treatment should have mitigated algae expected to become larger as a result of tion of freshwaters and coastal zones.

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11040 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0806112105 Carpenter Downloaded by guest on September 27, 2021