JPR Advance Access originally published online on December 4, 2006
Journal of Plankton Research 2007 29(1):1-6; doi:10.1093/plankt/fbl061
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
HORIZONS |
Using primary productivity as an index of coastal eutrophication: the units of measurement matter
Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USA
* Corresponding Author: vsmith{at}ku.edu
Received on August 24, 2006; accepted on October 24, 2006
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
Eutrophication is a serious environmental and economic problem in coastal marine ecosystems worldwide. It has recently been recommended that measurements of primary productivity, being a sensitive and accurate indicator of eutrophication, should be mandatory when monitoring and assessing the ecological status of coastal waters. The units of primary productivity chosen for eutrophication assessment will be very important because not all measures of primary productivity vary monotonically (or even straightforwardly) with changes in aquatic fertility. Volumetric expressions of primary productivity (rates of carbon fixation per unit volume of seawater) may prove to be the most sensitive and most reliable measures to use when evaluating the eutrophication status of coastal marine ecosystems. Another potential measure of primary productivity, the light-saturated rate of photosynthesis per unit Chlorophyll a (P:BChl) ratio, is unsuitable for the assessment of aquatic ecosystem responses to nutrient enrichment.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
Changes in primary productivity have been causally linked to the nutrient status of aquatic ecosystems for over a century. Brandt (Brandt, 1899
, 1902) first proposed that phytoplankton production must be dependent upon the supplies of nitrate-N and phosphate-P to natural waters (Ketchum et al., 1958). However, quantitative tests of Brandt's hypothesis could not be performed until suitable analytical tools for the measurement of primary productivity (the O2 and 14C methods), and for the measurement of water column concentrations of inorganic nutrients, could be developed.
More than 50 years after Brandt's seminal papers, Ketchum et al. (Ketchum et al., 1958) published data from shipboard nutrient enrichment bioassays that unequivocally revealed nutrient limitation of phytoplankton productivity in natural seawater communities, as revealed by both the oxygen and radiocarbon techniques. A decade later, Ketchum (Ketchum, 1970) confirmed the existence of very strong links between nutrient availability and phytoplankton production by demonstrating a tight relationship between the concentrations of phosphorus and phytoplankton biomass [measured as chlorophyll a (Chla)] in seawater samples taken along a broad eutrophication gradient from oligotrophic coastal and open ocean sites to polluted estuaries.
Both our knowledge and our ability to manage aquatic eutrophication have expanded tremendously during the intervening three decades; this knowledge has been summarized in several synthetic reviews (Smith et al., 1999; Smith, 2003, 2006). It can now be argued that, in general, the results of nutrient over-enrichment tend to be negative, with beneficial effects being rare or accidental (Fisher et al., 1995). In particular, eutrophication often has a strongly negative economic dimension (Segerson and Walker, 2002): in England and Wales, for example, the damage costs of freshwater eutrophication alone have been estimated to be £75–114 million per year (Pretty et al., 2003). Similarly, the economic consequences of estuarine and coastal marine eutrophication can be very substantial, and are expected to increase over time worldwide as human population numbers grow and move into coastal communities.
Human-derived nutrient inputs are thus a growing threat to coastal zone ecosystems (Vidal et al., 1999; Rabalais and Nixon, 2002; Joye et al., 2006). Stressing the importance of coastal water quality protection, Andersen et al. (2006) have recently suggested that eutrophication be defined as ‘the enrichment of water by nutrients, especially nitrogen and/or phosphorus and organic matter, causing an increased growth of algae and higher forms of plant life to produce an unacceptable deviation in structure, function and stability of organisms present in the water and to the quality of water concerned, compared to reference conditions.’ In their opinion, this re-definition will lead to revisions of existing coastal zone monitoring studies; and, because primary productivity measurements are quantitative indicators of photoautotroph growth, Andersen et al. suggest that 14C-based primary productivity measurements should be mandatory in monitoring networks and should be included as a parameter in pan-European eutrophication assessments.
Rates of primary productivity indeed have been included as a component of many trophic state assessment frameworks for freshwater and marine ecosystems worldwide (Rodhe, 1970; Andersen et al., 2006). However, I wish to stress in this paper that the units of primary productivity that are chosen for use in future monitoring and restoration efforts will be very important, because not all measures of primary productivity vary monotonically (or even straightforwardly) with changes in aquatic fertility.
|
EFFECTS OF EUTROPHICATION ON AREAL PRODUCTIVITY |
|---|
|
TOPABSTRACTINTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
Notable among the changes caused by aquatic eutrophication is a rapid initial increase in areal (integrated) primary productivity (
A: g C m–2 year–1, or mg C m–2 day–1), which then slows as phytoplankton biomass accumulates in the water column, and as the depth of the euphotic zone diminishes due to increasing light attenuation (Bannister, 1974). This nonlinear response of integral photosynthesis to eutrophication was demonstrated in the Laurentian Great Lakes by Vollenweider et al. (Vollenweider et al., 1974), who reported a strong hyperbolic relationship between annual areal primary productivity and areal phosphorus loading (LP g P m–2 year–1),
|
|
|
|
Similar relationships have been observed in a wide variety of estuarine and coastal marine ecosystems. For example, an analysis of 14 estuarine ecosystems worldwide by Howarth (1993) revealed a strongly curvilinear response of A to areal nitrogen loading (LN, g N m–2 year–1), and similar results [Equation (3)] were reported in an extensive series of comparative studies made by Nixon et al. (Nixon et al., 1996; Nixon, 1992, 1997),
|
|
) also recently extended the analysis of Nixon (Nixon, 1992) to include primary productivity measurements from the Long Island Sound (USA).
However, the nonlinearity of equations (1–3) and similar relationships raises potential concerns about using areal primary productivity as a core index of eutrophication in coastal systems, many of which are already highly nutrient-enriched and are thus biased towards the upper, flatter portion of the curve (Kelly, 2001). Even within a single aquatic ecosystem, the response of A to changes in nutrient availability saturates very rapidly. For example, in Lake Washington (USA), daily rates of areal primary productivity reached a maximum value at total phosphorus (TP) concentrations of ca. 1 µM, and remained relatively unchanged up through concentrations that exceeded 2 µM (Fig. 1). A thus was a very poor indicator of Lake Washington's response to human-driven changes in nutrient loading, particularly during the critically important nutrient diversion period during 1963–68, when wastewater effluents were progressively removed from the lake (Edmondson, 1991), and the lake's subsequent return to acceptable water quality conditions.
|
|
EFFECTS OF EUTROPHICATION ON VOLUMETRIC PRODUCTIVITY |
|---|
|
TOPABSTRACTINTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
In contrast to
A, volumetric expressions of primary productivity tend to track changes in nutrient loading and algal biomass much more predictably and sensitively. For example, Ketchum et al. (Ketchum et al., 1958) found that gross photosynthesis (mg C m–3 h–1, measured using dark and light oxygen bottle methods at a constant incident irradiance of 1500 foot-candles (
300 µmol photons m–2 s–1) by marine phytoplankton was linearly correlated with water column concentrations of Chla during all seasons of the year.
A similar measure of primary productivity, Aopt (mg C m–3 day–1), is the light-saturated, maximum volumetric rate of photosynthesis observed in a standard vertical productivity profile. Although both Vallentyne (Vallentyne, 1969) and Smith (Smith, 1979) have stressed the sensitivity of Aopt to eutrophication, the strong relationships that exist between nutrients, chlorophyll, and volumetric rates of photosynthesis have unfortunately remained relatively neglected. However, the critical distinction between the responses of integral and volumetric rates of photosynthesis to eutrophication can clearly be seen in the case of Lake Washington (Fig. 2). In contrast to the behavior of integral photosynthesis (Fig. 1), Aopt was extremely sensitive to the rapid cultural eutrophication that occurred between 1958 and 1963, and Aopt was almost linearly dependent upon total phosphorus concentrations in the lakewater during Lake Washington's recovery after the imposition of nutrient loading controls (Fig. 2).
|
|
EFFECTS OF EUTROPHICATION ON P:BChl RATIOS |
|---|
|
TOPABSTRACTINTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
A recent paper by Yoshiyama and Sharp (Yoshiyama and Sharp, 2006
) focused on a third potential index of autotrophic responses to nutrient enrichment, the P:BChl ratio [mg C (mg Chla)–1 day–1]. This index was calculated as the ratio of maximum volumetric primary productivity, as measured along a photon flux gradient in an on-deck incubator, to Chla. These authors evaluated phytoplankton productivity responses to variations in nutrient loading to the Delaware Estuary (USA), using an extensive 26-year database. They sought but did not find strong relationships between P:BChl and water column nutrient concentrations that ranged from < 0.1 to ca. 6 µmol P L–1 as dissolved inorganic phosphate, and from << 10 to ca. 200 µmol N L–1 as dissolved inorganic nitrogen. The P:BChl ratio proved to be quite invariant in this system, except at low nutrient concentrations.
Based on measurements of primary productivity expressed in terms of P:BChl ratios, Yoshiyama and Sharp (Yoshiyama and Sharp, 2006) concluded that ‘decreased phytoplankton responses were found in overenriched waters; in particular, primary production was depressed in the urban river where anthropogenic influences were strongest. These findings indicate that high nutrient concentrations do not stimulate primary production; in contrast, it appears that high nutrients are indicative of inhibition.’
Yoshiyama and Sharp's very surprising conclusions would at first appear to conflict strongly with our current knowledge of the strong positive links that exist between primary productivity and nutrient enrichment. However, I conclude that Yoshiyama and Sharp's conclusions followed necessarily from the choice of P:BChl ratios as their focal index of phytoplankton response to nutrient enrichment. Eutrophication is known to cause pronounced shifts in phytoplankton species composition, and P:BChl ratios can respond to these compositional shifts because of consequent alterations in the ratio of Photosystem II:Photosystem I (PSII:PSI) within the phytoplankton community. Such changes in PSII:PSI can in turn alter photosynthetic rates per unit Chla (Falkowski et al., 1981; Silsbe et al., 2006), making the P:BChl ratio a noisy and potentially insensitive indicator of nutrient enrichment.
The inability of P:BChl ratios to sensitively track directional changes in nutrient loading is underscored by data from Lake Washington, which revealed that phytoplankton P:BChl ratios did not change in a consistent or predictable manner during the lake's eutrophication, restoration, and subsequent recovery between 1958 and 1975 (Fig. 3).
|
Although Yoshiyama and Sharp (Yoshiyama and Sharp, 2006
) reported a very modest variance in P:BChl ratios, measurements of primary productivity in the Delaware Estuary varied by almost two orders of magnitude; areal photosynthesis, for example, varied from < 100 to ca. 6000 mg C m–2 day–1. As has been found in nearby Chesapeake Bay (Boynton et al., 1995), and in many other estuarine and coastal marine systems, primary productivity in the Delaware Estuary can be shown to be significantly and positively correlated with nutrient enrichment. A plot of the 26-year spring and summer averages from Table 1 in Yoshiyama and Sharp (Yoshiyama and Sharp, 2006) is very revealing (Fig. 4): their light-saturated volumetric measure of photosynthesis (VPROD) exhibited consistently strong and positive correlations with Chla concentrations in this system; areal photosynthesis (APROD) and the P:BChl ratio did not.
|
The very limited utility and explanatory power of P:BChl ratios in eutrophication assessment can be further demonstrated using data obtained from freshwater ecosystems. The measurements of Aopt and Chla compiled in Table 1 of Smith (Smith, 1979
) reveal that P:BChl ratios varied only slightly from a value of 22.7 mg C (mg Chla)–1 day–1 in oligotrophic Lake Superior (average algal biomass: 1.0 µg L–1 Chla), to a value of 18.6 mg C (mg Chla)–1 day–1 in hypereutrophic Loch Leven (average algal biomass: 96 µg L–1 Chla). Lemoalle (Lemoalle, 1981) observed extremely low variance in phytoplankton P:BChl ratios in Lake Chad (Africa) over an extremely wide range of integrated euphotic zone chlorophyll contents (<5 to >300 mg Chla m–2); 90% of the total variability in all 132 measurements of areal primary productivity from Lake Chad could be accounted for by variations in algal biomass alone! Similarly, Morabito et al. (Morabito et al., 2004) observed relatively small variations in the P:BChl ratio during their recent study of carbon assimilation in three subalpine Italian lakes. In unproductive Lago Maggiore (TP = 0.3 µM) and Lago Mergozzo (TP = 0.3 µM), P:BChl ratios in June–July averaged 3.89 and 4.89 mg C (mg Chla)–1 h–1, respectively; the mean P:BChl ratio in eutrophic Lago Varese (TP = 1 µM) was very similar, at 3.26 mg C (mg Chla)–1 h–1. |
CONCLUSIONS |
|---|
|
TOPABSTRACTINTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
Measurements of nutrient concentrations (especially total nitrogen and total phosphorus), algal biomass (using concentrations of Chla and/or algal biovolume), and Secchi disk transparency will continue to be essential parameters in future efforts to manage and monitor coastal zone eutrophication. Andersen et al. (Andersen et al., 2006
) have proposed that measurements of primary productivity should be added as a mandatory component of these efforts. If their recommendation is accepted, I conclude that areal or volumetric expressions of primary productivity should be measured and reported. Of these two parameters, I suggest that volumetric productivity may provide a more sensitive and a more valuable tool to monitor both the current and future trophic states of estuarine, coastal, and offshore marine ecosystems; this is a testable hypothesis. In contrast, the P:BChl ratio is without question a very sensitive indicator of phytoplankton physiological state which can provide valuable information for aquatic scientists in many other contexts. However, I conclude that it is not a satisfactory indicator of the trophic state of the waterbody which the phytoplankton inhabits. I therefore do not recommend the use of P:BChl ratios as a eutrophication indicator in the European Union Water Framework Directive's developing frameworks for coastal water management and protection, or indeed for any other regulatory activity in the world's coastal waters.
|
ACKNOWLEDGEMENTS |
|---|
I thank Ed Dettmann and Bob Carlson for their helpful comments on this manuscript. This research was supported in part by a contract to the Great Lakes Environmental Center from the United States Environmental Protection Agency. However, the views and conclusions expressed in this paper are those of the author alone, and do not necessarily reflect either the opinions or the policies of the USEPA.
|
Notes |
|---|
Communicating editor: R.P. Harris
Written responses to this article should be submitted to Roger Harris at rph@pml.ac.uk within two months of publication. For further information, please see the Editorial ‘Horizons’ in Journal of Plankton Research, Volume 26, Number 3, Page 257.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONEFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...EFFECTS OF EUTROPHICATION ON...CONCLUSIONSREFERENCES |
|---|
Andersen J. H., Schlüter L., Ærtebjerg G. (2006) Coastal eutrophication: recent developments in definitions and implications for monitoring strategies. J. Plankton Res. 28 621–628.
Bannister T. T. (1974) Production equation in terms of chlorophyll concentration, quantum yield, and upper limit to production. Limnol. Oceanogr. 19 1–12.
Boynton W. R., Garber J. H., Summers R., et al. (1995) Inputs, transformations, and transport of nitrogen and phosphorus in Chesapeake Bay and selected tributaries. Estuaries 18 285–314.[Medline]
Brandt W. (1899) Über den Stoffwechsel im Meere. Wiss Meeresunters., Abt. Keil 4 213–230.
Brandt W. (1902) Über den Stoffwechsel im Meere. Wiss Meeresunters., Abt. Keil 6 23–79.
Edmondson W. T. (1991) The Uses of Ecology: Lake Washington and BeyondSeattle, WA University of Washington Press.
Falkowski P. G., Owens T. G., Ley A. C., et al. (1981) Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol. 68 969–973.
Fisher T. R., Melack J. M., Grobbelaar J. U., et al. (1995) Nutrient limitation of phytoplankton and eutrophication of inland, estuarine, and marine waters. In Tiessen H. (Ed.). Phosphorus in the Global EnvironmentNew York Wiley pp. 301–322.
Goebel N. L., Kremer J. N., Edwards C. A. (2006) Primary production in Long Island Sound. Estuar. Coasts 29 232–245.
Howarth R. W. (1993) The role of nutrients in coastal waters. Washington, DC National Academy Press 177–202 Report from the National Research Council Committee on Wastewater Management for Coastal Urban Areas.
Eutrophication of freshwater and marine ecosystems. In Joye S. B., Smith V. H., Howarth R. W. (Eds.), et al. Limnol. Oceanogr. (2006) 51(1, part 2) pp. 351–800.
Kelly J. (2001) Nitrogen effects on coastal marine ecosystems. In Follett R. F. and Hatfield J. L. (Eds.). Nitrogen in the Environment: Sources, Problems and ManagementAmsterdam Elsevier.
Ketchum B. H. (1970) Eutrophication of estuaries. Eutrophication: Causes, Consequences, CorrectivesWashington, DC National Academy of Sciences pp. 197–209.
Ketchum B. H., Ryther J. H., Yentsch C. S., et al. (1958) Productivity in relation to nutrients. J. Conseil. Rapport Mer. 144 132–140.
Lemoalle J. (1981) Photosynthetic production and phytoplankton in the euphotic zone of some African and temperate lakes. Rev. Hydrobiol. Trop. 14 31–37.
Morabito G., Hamza W., Ruggiu D. (2004) Carbon assimilation and phytoplankton growth rates across the trophic spectrum: an application of the chlorophyll labeling technique. J. Limnol. 63 33–43.
Nixon S. W. (1992) Quantifying the relationship between nitrogen input and the productivity of marine ecosystems. Proceedings of Advanced Marine Technology Conference In Takahashi M., Nakata K., Parsons T. R. (Eds.). Tokyo, Japan 5 57–83.
Nixon S. W. (1997) Prehistoric nutrient inputs and productivity in Narragansett Bay. Estuaries 20 253–261.[CrossRef][ISI]
Nixon S. W., Ammerman J. W., Atkinson L. P., et al. (1996) The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry 35 141–180.
Pretty J. N., Mason C. F., Nedwell D. B., et al. (2003) Environmental costs of freshwater eutrophication in England and Wales. Environ. Sci. Technol. 37 201–208.[Medline]
In Rabalais N. and Nixon S. W. (Eds.). Dedicated issue. Nutrient overenrichment in coastal waters: global patterns of cause and effect. Estuaries (2002) 25 639–900.[ISI]
Rodhe W. (1970) Crystallization of eutrophication concepts in Northern Europe. Eutrophication: Causes, Consequences, CorrectivesWashington, DC National Academy of Sciences pp. 50–64.
Silsbe G. M., Hecky R. E., Guildford S. J., et al. (2006) Variability of chlorophyll a and photosynthetic parameters in a nutrient-saturated tropical great lake. Limnol. Oceanogr. 51 2052–2063.
Segerson K. and Walker D. (2002) Nutrient pollution: an economic perspective. Estuaries 25 797–808.[ISI]
Smith V. H. (1979) The nutrient dependence of primary productivity in lakes. Limnol. Oceanogr. 24 1051–1064.
Smith V. H. (2003) Eutrophication of freshwater and marine ecosystems: a global problem. Environ. Sci. Pollut. Res. 10 126–139.
Smith V. H. (2006) Responses of estuarine and coastal marine phytoplankton to nitrogen and phosphorus enrichment. Limnol. Oceanogr. 51(1, part 2) 377–384.
Smith V. H., Tilman G. D., Nekola J. C. (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ. Pollut. 100 179–196.[CrossRef]
Vallentyne J. R. (1969) The process of eutrophication and criteria for trophic state determination. Modelling the Eutrophication ProcessGainesville University of Florida pp. 57–67.
Vidal M., Duarte C. M., Sánchez M. C. (1999) Coastal eutrophication research in Europe: progress and imbalances. Mar. Pollut. Bull. 38 851–854.[CrossRef][ISI]
Vollenweider R. A., Munawar M., Stadelmann P. (1974) A comparative review of phytoplankton and primary production in the Laurentian Great Lakes. J. Fish. Res. Bd. Can. 31 739–762.
Yoshiyama K. and Sharp J. H. (2006) Phytoplankton response to nutrient enrichment in an urbanized estuary: apparent inhibition of primary production by overeutrophication. Limnol. Oceanogr. 51(1, part 2) 424–434.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||