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HORIZONS
Using primary productivity as an index
of coastal eutrophication: the units
of measurement matter
VAL H. SMITH*
DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY, UNIVERSITY OF KANSAS, LAWRENCE, KS
66045, USA
*CORRESPONDING AUTHOR: [email protected]
Received August 24, 2006; accepted in principle September 28, 2006; accepted for publication October 24, 2006; published online
December 4, 2006
Communicating editor: R.P. Harris
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.
I N T RO D U C T I O N
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.
Written responses to this article should be submitted to Roger Harris at [email protected] within two months of publication. For further
information, please see the Editorial ‘Horizons’ in Journal of Plankton Research, Volume 26, Number 3, Page 257.
doi:10.1093/plankt/fbl061, available online at www.plankt.oxfordjournals.org
# The Author 2006. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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primary productivity (SA: g C m22 year21, or mg
C m22 day21), 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 m22 year21),
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.
SA ¼
ð4200 LP0:6 Þ
:
ð9 þ 10 LP0:6 Þ
ð1Þ
These authors also reported a similarly hyperbolic
relationship between annual areal primary productivity
and yearly average concentrations of Chla in the water
column (Chla, mg L21),
SA ¼
ð483 Chla1:33 Þ
:
ð9 þ 1:15 Chla1:33 Þ
ð2Þ
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 SA to areal nitrogen loading (LN,
g N m22 year21), 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),
log SA ¼ 0:442 log DIN þ 2:332;
ð3Þ
where DIN is the estimated annual load of dissolved
inorganic nitrogen per unit area (mol N m22 year21).
Goebel et al. (Goebel et al., 2006) 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 SA 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)
E F F E C T S O F E U T RO P H I C AT I O N
O N A R E A L P RO D U C T I V I T Y
Notable among the changes caused by aquatic eutrophication is a rapid initial increase in areal (integrated)
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Fig. 1. Relationship between integral primary productivity (SA,
mg C m22 day21) and total phosphorus concentrations in Lake
Washington (USA) during its eutrophication and recovery, 1958– 75.
Data from Fig. 7B in Smith (Smith, 1979).
Fig. 2. Relationship between volumetric primary productivity (Aopt,
mg C m23 day21) and total phosphorus concentrations in Lake
Washington (USA) during its eutrophication and recovery, 1958–75.
Data from Table 1 in Smith (Smith, 1979).
concentrations of ca. 1 mM, and remained relatively
unchanged up through concentrations that exceeded
2 mM (Fig. 1). SA 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.
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).
E F F E C T S O F E U T RO P H I C AT I O N
O N VO L U M E T R I C
P RO D U C T I V I T Y
E F F E C T S O F E U T RO P H I C AT I O N
O N P : B C h l R AT I O S
In contrast to SA, 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 m23 h21,
measured using dark and light oxygen bottle methods
at a constant incident irradiance of 1500 foot-candles
(300 mmol photons m22 s21) 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 m23 day21), 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.
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)21 day21]. 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 mmol P L21 as dissolved inorganic phosphate, and from 10 to ca. 200 mmol N L21 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
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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
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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 m22 day21. As has been found
in nearby Chesapeake Bay (Boynton et al., 1995), and in
Fig. 4. Relationships between concentrations of chlorophyll a and (A)
APROD, areal primary productivity; (B) VPROD, light-saturated
volumetric productivity; and (C) the P:BChl ratio in the Delaware
Estuary (USA). These acronyms and data are from Table 1 in
Yoshiyama and Sharp (Yoshiyama and Sharp, 2006). APROD and
VPROD were estimated by these authors from samples taken at five
geographic regions along a longitudinal transect in the Delaware
Estuary; these samples were illuminated at six irradiance levels in a
deck incubator for 24 h using the 14C technique.
Fig. 3. Relationship between P:BChl ratios (calculated as the quotient
between Aopt and Chla) and total phosphorus concentrations in Lake
Washington (USA) during its eutrophication and recovery, 1958– 75.
Data from Table 1 in Smith (Smith, 1979) and V. H. Smith
(unpublished data).
4
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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)21 day21 in oligotrophic Lake
Superior (average algal biomass: 1.0 mg L21 Chla), to a
value of 18.6 mg C (mg Chla)21 day21 in hypereutrophic
Loch Leven (average algal biomass: 96 mg L21 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 m22); 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 ¼ 0.3 mM) and Lago Mergozzo
(TP ¼ 0.3 mM), P:BChl ratios in June–July averaged 3.89
and 4.89 mg C (mg Chla)21 h21, respectively; the mean
P:BChl ratio in eutrophic Lago Varese (TP ¼ 1mM) was
very similar, at 3.26 mg C (mg Chla)21 h21.
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.
CONCLUSIONS
Brandt, W. (1899) Über den Stoffwechsel im Meere. Wiss Meeresunters.,
Abt. Keil, 4, 213– 230.
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
Brandt, W. (1902) Über den Stoffwechsel im Meere. Wiss Meeresunters.,
Abt. Keil, 6, 23–79.
AC K N OW L E D G E M E N T S
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.
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