Marine Pollution Bulletin 55 (2007) 74–90

www.elsevier.com/locate/marpolbul

Assessing the impact of nutrient enrichment in estuaries:

Susceptibility to eutrophication
a,*
S.J. Painting , M.J. Devlin a, S.J. Malcolm a, E.R. Parker a, D.K. Mills a, C. Mills a,
P. Tett b, A. Wither c, J. Burt d, R. Jones e, K. Winpenny a
a
The Centre for Environment, Fisheries and Aquaculture Science (Cefas), Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK
b
School of Life Sciences, Napier University, 10 Colinton Road, Edinburgh EH10 5DT, Scotland, UK
c
The Environment Agency (EA), Richard Fairclough House, Knutsford Road, Warrington WA4 1HG, UK
d
English Nature (EN), Northminster House, Peterborough PE1 1UA, UK
e
Countryside Council for Wales (CCW), Maes-y-Ffynnon, Penrhosgarnedd, Bangor, Gwynedd LL57 2DW, UK

Abstract

The main aim of this study was to develop a generic tool for assessing risks and impacts of nutrient enrichment in estuaries. A simple
model was developed to predict the magnitude of primary production by phytoplankton in different estuaries from nutrient input (total
available nitrogen and/or phosphorus) and to determine likely trophic status. In the model, primary production is strongly influenced by
water residence times and relative light regimes. The model indicates that estuaries with low and moderate light levels are the least likely
to show a biological response to nutrient inputs. Estuaries with a good light regime are likely to be sensitive to nutrient enrichment, and
to show similar responses, mediated only by site-specific geomorphological features. Nixon’s scale was used to describe the relative tro-
phic status of estuaries, and to set nutrient and chlorophyll thresholds for assessing trophic status. Estuaries identified as being eutrophic
may not show any signs of eutrophication. Additional attributes need to be considered to assess negative impacts. Here, likely detriment
to the oxygen regime was considered, but is most applicable to areas of restricted exchange. Factors which limit phytoplankton growth
under high nutrient conditions (water residence times and/or light availability) may favour the growth of other primary producers, such
as macrophytes, which may have a negative impact on other biological communities. The assessment tool was developed for estuaries in
England and Wales, based on a simple 3-category typology determined by geomorphology and relative light levels. Nixon’s scale needs to
be validated for estuaries in England and Wales, once more data are available on light levels and primary production.
 2006 Elsevier Ltd. All rights reserved.

Keywords: Estuaries; Nutrients; Light; Primary production; Eutrophication

1. Introduction primary concern is the susceptibility of estuaries to eutro-

Nutrients and their role in changing the trophic status of
aquatic environments have been the subject of much
research, but the impact of nutrients on the functioning
of estuaries and their associated habitats is still poorly
understood. This uncertainty has implications for the reli-
able protection and conservation of estuarine systems. Of
*
Corresponding author. Tel.: +44 1502 527707; fax: +44 1502 526507.
E-mail address: s.j.painting@cefas.co.uk (S.J. Painting).
phication, where eutrophication is defined as ‘‘enrichment
of water by nutrients especially compounds of nitrogen
and phosphorus, causing an accelerated growth of algae
and higher forms of plant life to produce an undesirable
disturbance to the balance of organisms and the quality
of the water concerned’’ (Urban Wastewater Treatment
Directive, UWWTD, C.E.C., 1991, 2000).
Over the past two decades, considerable effort has been
directed towards the development of tools for assessing the
risks and impacts of eutrophication. In general, three
approaches have been adopted, viz. the setting of standards

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doi:10.1016/j.marpolbul.2006.08.020
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90 75

or thresholds based on available data and expert judge- indicators of the negative impacts of nutrient enrichment
ment, the establishment of empirical relationships and the on estuarine ecosystems include the development of blooms
development of numerical modelling tools. of toxic algae, increased growth of epiphytic algae, the loss
For freshwater, the OECD (1982) proposed a simple of submerged vegetation, and the growth of macroalgae,
system of thresholds for assessing eutrophic status (Table all of which have potential consequences for estuarine
1). This approach was extended to coastal water (CSTT, habitats and resource utilisation (see Bricker et al., 1999;
1994, 1997) and to estuaries, coastal and offshore waters Tett et al., 2006).
(OSPAR, Table 1). In Europe, ongoing development of Empirical relationships between nutrients and the
assessment tools has been undertaken by OSPAR and growth of primary producers have been developed in
under EU directives such as the Water Framework Direc- numerous studies. For example, Gowen et al. (1992) stud-
tive (WFD). These include the development of Ecological ied the relationship between nitrate concentrations and
Quality elements and objectives for monitoring nutrient phytoplankton chlorophyll a biomass in Scottish waters,
enrichment and potential eutrophication effects in coastal and showed that chlorophyll yield could be predicted from
waters (OSPAR 2005; Painting et al., 2005). In the US, dissolved available inorganic nitrogen (DAIN) and inor-
the national eutrophication model includes primary and ganic phosphate (DAIP). Using data from a variety of
secondary symptoms of eutrophication (Bricker et al., marine ecosystems, Nixon et al. (1996) established a simple
1999). Few attempts have been made to include estimates relationship for predicting annual net primary production
of primary production in assessments. Rodhe (1969) pro- from input of dissolved inorganic nitrogen (DIN). These
posed net annual primary production thresholds for assess- (and other) predictive relationships are useful for under-
ing eutrophic status of ‘naturally eutrophic’ and ‘polluted’ standing the potential response to nutrient enrichment,
freshwater (>75 and >350 g C m2 y1 respectively, Table and are likely to contribute towards the ongoing develop-
1). For coastal marine waters, Nixon (1995) proposed a ment of tools for assessing eutrophication in coastal and
similar scale for assessing trophic status. However, these marine waters.
descriptors of eutrophic status have no direct bearing on The simplest models for eutrophication aim only to pre-
the term ‘‘eutrophication’’, as defined by the UWWTD dict the value of an easily observed variable, such the bio-
(C.E.C., 1991). Additional attributes need to be considered mass of phytoplankton. The UK’s Comprehensive Studies
to assess negative impacts. Many assessments consider oxy- Task Team (CSTT, 1994, 1997) developed a simple box
gen concentrations below about 6 mg/l to be indicative of model to calculate phytoplankton yield (in terms of bio-
negative impacts. Other attributes likely to be important mass) from nutrient inputs. Models such as the CSTT
model may be used to screen ecosystems for actual or
Table 1
potential eutrophication. Models of increasing complexity
Existing ‘thresholds’ for assessing eutrophic status for assessing the impact of nutrient enrichment in estua-
Variable Threshold Units
rine, coastal and offshore waters include coupled physi-
cal–biological models (Tett, 2000; Baretta-Bekker and
OECD (1982)
Mean total P >35.0 lg l1
Baretta, 1997; Moll and Radach, 2003) and are currently
Mean Chl >8.0 lg l1 under review by OSPAR.
Max. Chl >25 lg l1 For estuaries, susceptibility to nutrient enrichment is
Mean Secchi depth <3.0 m controlled by a wide variety of factors influenced by the
Min Secchi depth <1.5 m physical setting, the hydro-dynamic regime, and biological
CSTT (1994, 1997) processes (National Research Council, 2000). Although the
Winter DAIN >12 lM detailed response of estuaries to nutrients is system specific,
Summer max Chl >10 lg l1
there are relatively few pathways that can lead to a pertur-
OSPAR (2001, 2003) bation of the balance of organisms and water quality. In
Winter DIN & /or DIP >50% above background with defaults of general terms, subject to light availability, nutrient input
DIP > 0.8 lM
DIN > 15 lM
leads to growth of opportunistic fast growing primary
Winter N/P ratio >25:1 at:at producers and the accumulation of extra biomass. The
Growing season Chl >50% above background primary producers may be opportunistic green algae,
Annual net primary production epiphytes or phytoplankton. The consequence is a modifi-
Freshwater cation to the make up of the plant community as a result
Rodhe (1969) >75 g C m2 y1 or of competition or interference. For example, excessive
>350 g C m2 y1 (see text) phytoplankton growth may increase water turbidity, which
Seawater
restricts the availability of underwater light and may
Nixon (1995) >300 g C m2 y1
change the depth distribution of macroalgae. This has
The OECD proposed annual means, the CSTT and OSPAR recom-
important implications for the structure and functioning
mended seasonal means. OSPAR background concentrations are region
and salinity specific. Min = minimum, max = maximum, Chl = chloro- of estuarine food webs. These changes can ultimately lead
phyll, D = dissolved, A = available, I = inorganic, N = nitrogen, P = to the degradation of water quality for animal or human
phosphorus. use.
76 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90
The objective of this study was to develop a generic tool
for assessing the risks and impacts of nutrient enrichment
in different types of estuaries based on the growth of phy-
toplankton, which usually provide the first indication of
biological response to nutrient enrichment in estuaries.
Field data were obtained for estuaries in England and
Wales, and analysed to determine predictive relationships.
The CSTT modelling approach was adapted and expanded
to predict the magnitude of potential primary production
by the phytoplankton community in response to nutrient
input. The improved model was used to develop an assess-
ment tool which could be applied to any estuary, even in
the absence of detailed field data.
2. Methods
Estuaries in England and Wales were divided into three
main categories based on geomorphological characteristics
and the relative light regime considered to be representative
of each of these categories (Table 2). Data on physico-
chemical characteristics and phytoplankton biomass were
obtained for estuaries in each of these categories to estab-
lish category-specific empirical relationships.
A simple screening model was developed to predict the
growth of phytoplankton in each of the estuarine cate-
gories in response to nutrient input. In the absence of
any other standards against which to compare the predic-
tions, the scale proposed by Nixon (1995) for assessing
trophic status from net annual primary production esti-
mates was applied, i.e., oligotrophic: 0–100 g C m2 y1,
mesotrophic: 101–300 g C m2 y1, eutrophic: 301–500 g
C m2 y1 or hypertrophic: >500 g C m2 y1. The pre-
dicted magnitude of primary production was used to set
thresholds for nutrient input in the different estuary catego-
ries. Predicted values were also used to estimate potential
changes in oxygen consumption rates, based on recommen-
dations by the CSTT (1994, 1997).
2.1. Field data
Total nitrogen and phosphorus loads (Mmol) per year
for all major estuaries in England and Wales were obtained
from Nedwell et al. (1999) and from the UK Environment
Agency, as required. Field data were obtained from the
Environment Agency for 43 estuaries in England and
Wales. Weekly and monthly data collected between 1980
and 2002 included water temperature (C), salinity,
suspended particulate material (SPM, mg l1), dissolved
Table 2
Estuary categories based on geomorphology (Davidson et al., 1991) and
relative light availability
Estuary category Geomorphological types Light levels
A Coastal plain Low
B Coastal plain Moderate
C Coastal plain, bar built, rias High
oxygen, nutrient concentrations (mg l1: nitrate, nitrite,
silicate and phosphate), and chlorophyll concentrations
(lg l1), used as a proxy for phytoplankton biomass. No
measurements of light were available. SPM data were used
as a rough index of relative light regimes. Data were plot-
ted for each estuary and in the different categories to iden-
tify ranges in field measurements, spurious data, temporal
and spatial trends, and differences between categories.
2.2. Description of the model
The model developed here (Fig. 1) was based on the
approach adopted by the Comprehensive Studies Task
Team (CSTT, 1994, 1997). The ecosystem is treated as a
well-mixed box of volume, V (m3). For estuaries, nutrient
inputs come from the land, rivers, atmosphere and adjacent
sea. All interactions with the sea are described by a single
parameter, E, the daily rate at which water is exchanged.
Nutrient losses are due to processes such as denitrification.
Eqs. (1)–(3) (below) define the original model, including
improvements by Tett et al. (2003, see Table 3), and Eq.
(4) is from Tett et al. (2003). In this study, primary produc-
tion (Eq. (5)) was considered to be the key predictor for the
effects of nutrient enrichment, and the model was devel-
oped to predict maximum net primary production using
predicted maximum chlorophyll biomass values and the
predicted (light-controlled) daily growth rates. The model
uses equilibrium nutrient concentrations to calculate max-
imum potential phytoplankton biomass. Important inputs
to the model are site-specific parameters on estuary vol-
ume, depth, exchange rates, nutrient loads/input (from
land, rivers, air and sea), nutrient losses, phytoplankton
inputs from adjacent coastal waters, microplankton loss
rates, and information on underwater optics (24-h mean
surface PAR, attenuation coefficients, and optical depth).
The maximum biomass of phytoplankton (Xmax) sup-
ported by nutrient enrichment is predicted by
X max ðmg m3 Þ ¼ X 0 þ q  S eq ð1Þ
where X0 is the concentration of phytoplankton chloro-
phyll (mg m3) in adjacent seawater, Seq is the equilibrium
nutrient concentration (lM), and q is the yield of phyto-
plankton from nutrient inputs. The CSTT recommended
the use of values of 1.05 mg Chl (mmol DAIN)1 and
50–100 mg Chl (mmol DAIP)1 (from Gowen et al.,
1992; see Edwards et al., 2003). Tett et al. (2003) recom-
mended a chlorophyll yield of 30 mg Chl (mmol DAIP)1,
which has been used in this study.
Equilibrium nutrient concentrations (Seq) for DAIN
(ammonium + nitrite + nitrate) and DAIP (reactive phos-
phate) are calculated using
S eq ðlMÞ ¼ S 0 þ ðsi =ðE  V ÞÞ ð2Þ
where S0 is the nutrient concentration (lM) in adjacent
seawater, si is the total of local inputs from sources other
than seawater (kmol d1), E is the water exchange rate
(d1) and V is the estuary volume (m3).
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90 77

Inputs: total nutrient input nutrient input

from land, rivers, from sea: Phytoplankton
discharges, air: S0 (µM) input from sea:
si (kmol d-1) X0 (mg chl m-3)
Exchange with sea
at relative rate E (d -1)

Losses
to denitri- si /(E x V)
fication etc V = estuary
volume
(%) (m3)
Losses
Equilibrium Phytoplankton to zooplankton,
Nutrient yield q (mg chl Biomass: Xmax deep water or
Concentrations: mmol-1 nutrient) (mg chl m-3) benthos: L (d-1)
Seq (µM)
Light-sensitive Oxygen
=
Growth*, µ (I)(d-1) consumption
(mg l-1)

Phytoplankton
production: Pmax
(g C m-2 y-1)
= =
* Note: Growth only occurs where µ(I) > E + L. Where µ(I) < E + L, X max values may be unrealistic

Fig. 1. Conceptual diagram to indicate model structure and information flow. The bold box indicates ambient (equilibrium) concentrations of nutrients in
the estuary, and the response by phytoplankton. Calculations of maximum phytoplankton production are sensitive to availability of light. Units are
explained in Eqs. (1)–(5) and in Table 3 (CSTT, 1997; Tett et al., 2003). Shaded boxes show outputs for assessing risks and impacts of nutrient enrichment:
phytoplankton production is used to assess trophic status using scales proposed by Nixon (1995); oxygen consumption rates (Eq. (7)) provide a
precautionary assessment of the likely impact of increased phytoplankton biomass on in situ oxygen concentrations.

Light controlled growth rates (lðIÞ) are calculated using
Eq. (3) and parameters given by Tett et al. (2003), viz.
0.006 d1 per micro-Einstein per m2 per second ((lE
m2 s1)1) for effective photosynthetic efficiency (aB)
under low light conditions, and 5 lE m2 s1 for compen-
sation irradiance (Ic):
lðIÞðd1 Þ ¼ aB  ðI  I c Þ
where a is effective photosynthetic efficiency (0.006 d1
B
I 1 ) at low illumination, I is photosynthetically available
radiation (PAR, lE m2 s1) averaged over 24 h and for
the upper mixed layer, and Ic is compensation PAR
(lE m2 s1).
Mean 24-h PAR (I, lE m2 s1) in the upper mixed
layer is calculated as follows (see Table 3):
 K d h
 for phytoplankton is 40 (whereas summer values are closer
I ðlE m2 s1 Þ ¼ ð1  m Þ  m  m  I  1  e ð4Þ
0 1 2 0
Kd  h
where I 0 is mean annual sea-surface 24-h solar radiation
(W m2), and m is used to convert mean surface radiation
into mean PAR in the upper mixed layer (see Table 3).
Light attenuation rates (Kd, m1) and mean depth of the
upper mixed layer (h, m) are key variables in Eq. (4), and
have a significant impact on estimates of PAR, and the
relative growth rates of microplankton (see Eq. (3)).
Light controlled growth rates are used in conjunction
with predicted phytoplankton biomass to calculate the
maximum production by phytoplankton (Pmax) using
P max ðg C m2 y1 Þ
¼ ðX max  lðIÞ  C : Chl  depth  365Þ=1000 ð5Þ
where Xmax is the maximum biomass of phytoplankton
(mg m3) supported by nutrient enrichment, lðIÞ is the
light controlled growth rate (d1), depth is given in metres
(m), and C:Chl is the carbon to chlorophyll ratio over an
ð3Þ
annual cycle (365 d).
2.3. Assumptions and default values
The model developed here is intended primarily for use
on an annual basis, although it is possible to use it on a sea-
sonal basis (below). In order to use or apply annual means
it was assumed that the annual carbon to chlorophyll ratio
to 25). Assuming 50% cloud cover and an average latitude
of 52N, the annual 24-h mean total surface irradiance was
calculated to be 150 W m2 s1. This falls within the range
(9.6–245 W m2) given by Gowen et al. (1995) and Peper-
zak et al. (1998). Low light availability theoretically
promotes diatom dominance. To develop the model, a
number of parameters had to be given default values. These
default values were based on a combination of data analy-
sis, expert judgement and sensitivity analysis. For assessing
the trophic status of an estuary, either the default value
may be used, or the actual values. On a category-specific
basis, the model is sensitive to the values used for light
attenuation rates, Kd, and water exchange rates, E.
78 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90

Table 3
Variables and parameters in the revised screening model (see also Tett et al., 2003)
Symbol Value Units
Model variables
Seq equilibrium nutrient concentration, = S0 + (si/(E Æ V)) lM
Xmax potential maximum chlorophyll concentration, = X0 + q Æ Seq mg m3
l(I) microplankton relative growth rate as a function of PAR, = aB Æ (I  Ic), d1
applied to mixed layer PAR I
Pmax potential maximum phytoplankton production, = ðX max  lðIÞ · C: g C m2 y1
Chl · depth · 365)/1000
Site-specific parameters
E exchange between estuary and the sea d1
L loss rate of microplankton due to mesozooplankton and benthic 0.0 d1
grazing, sinking, etc. (default value)
si total of nutrient input to the estuary from all sources except the sea kmol d1
S0 seawater (‘background’) nutrient concentration lM
V volume of estuary or of upper layer of estuary 106 m3
X0 seawater (‘background’) chlorophyll concentration mg m3
Standard parameters
q chlorophyll yield (from nitrogen) 1.1 mg Chl (mmol N)1
chlorophyll yield (from phosphorous) 30 mg Chl (mmol P)1
aB effective photosynthetic efficiency, = am X qNa  Qmax;a  ð1  gÞ=ð1 þ bÞ 0.006 d1(lE m2 s1)1
C:Chl carbon to chlorophyll ratio (annual) 40
Ic compensation irradiance, = (r0a Æ (1  g) + r0,h Æ g Æ (1 + ba))/(am Æ v) 5 lE m2 s1
Used to calculate standard parameters
am algal (chlorophyll-related), nutrient-replete, photosynthetic efficiency 0.042 mmol C (mg chl)1 d1
(lE m2 s1)1
b rate of increase of (microplankton) respiration with growth, 1.4
= ba Æ (1 + bh Æ g) + bh Æ g
ba rate of increase of (autotroph) respiration with growth 0.5
bh rate of increase of (heterotroph) respiration with growth 1.5
g ‘heterotroph’ fraction = microheterotroph carbon biomass  0.4
total microplankton biomass
Qmax,a maximum autotroph nitrogen content 0.20 mmol N (mmol C)1
x N
qa autotroph chlorophyll:nitrogen ratio 3.0 mg Chl (mmol N)1
r0,a autotroph basal respiration (at zero growth) 0.05 d1
r0,h heterotroph basal respiration (at zero growth) 0.07 d1
Submarine optics  K h 
I 24-h mean PAR (in mixed layer), = ð1  m0 Þ  m1  m2  I 0  1e d
lE m2 s1
K d h
I mean annual sea-surface 24-h solar radiation 150 W m2
0
m0 sea albedo 0.06
m1 conversion from total solar energy to PAR photons 0.46 · 4.15 lE J1
m2 fraction of the surface PAR that is penetrating light 0.4
h thickness of mixed layer m
Kd diffuse attenuation for PAR m1

Light attenuation (Kd) is used in the model to calculate
optical depth (Kd · h, where h is the mean depth (in metres)
of the upper mixed layer, see Eq. (4)). The depth of the
upper mixed layer is assumed to be equivalent to the mean
depth (m) of the estuary. This assumes no stratification. A
caveat for h is that within an estuary, brief periods of strat-
ification may occur (depending on freshwater input and
tidal state). This will effectively reduce h and therefore
the optical depth.
Water exchange rates, E, have important implications
for many model variables and site-specific parameters,
including losses of nitrogen which would otherwise be
available for uptake by phytoplankton. Relative water res-
idence times in the different estuary categories (Table 4)
were used to estimate water exchange rates (d1, Table 4)
based on data presented by Tett et al. (2003). Water resi-
dence times were used to estimate N losses due to denitri-
fication (Table 4) using the relationship given by Nixon
et al. (1996), and applied directly to data on total nitrogen
loading. Where nutrient uptake by benthic diatoms is
important, these losses should be included here. They were
also used to estimate losses due to consumption by higher
trophic levels and sinking of particulate material. It was
assumed that longer residence times would be associated
with higher losses due to such factors. Microplankton loss
rates (L) were estimated to range from 0.3 to 1 for the dif-
ferent estuary types. Initial validation of the model indi-
cated that these values were too high. To allow potential
maximum biomass to be realised in the model, default
values were set to zero for all estuary categories.
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90
Table 4
Guidelines followed for using water residence time (Rogers et al., 2003) to estimate water exchange rates (E, d1, from Tett et al., 2003), nitrogen losses due
to denitrification (from Nixon et al., 1996), and nitrogen losses due to microplankton grazing and/or sinking (L, d1)
Estuary category Relative water Estimated water
residence times exchange rate (E, d1)
A Months 0.05
B Weeks 0.1
C Days 0.3
The model developed here is sensitive to the input of
nutrients and phytoplankton from the sea. Default values
were set at 20% of the thresholds (10.3 lM nitrogen,
0.2 lM phosphorus, 10 lg Chl l1) recommended by the
North Sea Status Report and the CSTT (1994, 1997).
The default values were therefore set at 2 lM for nitrogen,
0.04 lM phosphorus and 2 lg Chl l1 (mg Chl m3) for
phytoplankton.
2.4. Model performance
Ten estuaries were selected for testing the performance
of the model – 2 each from categories A and B, and six
from category C (see Figs. 5 and 6). Six estuaries were
selected for detailed testing and validation of the model,
due to concerns about their conservation status. Three
were from category C: Milford-Haven, the Mawddach,
and the Exe; three were from category B: the Stour-Orwell,
Plymouth Sound/Tamar, and The Wash. In all cases, only
minimal data were available. It was therefore not possible
to test all the default values used in the model, or model
results.
Data on total areas, mean depths and mean water resi-
dence times of test estuaries were obtained from Rogers
et al. (2003). Mean seawater concentrations of total nitro-
gen and phosphorus were taken from Parr et al. (1999).
Mean chlorophyll concentrations in adjacent coastal
waters were estimated from available data collected by
the Environment Agency.
2.5. Potential impacts of phytoplankton yield on oxygen
concentrations
The potential detrimental impact of phytoplankton yield
(in terms of chlorophyll) on oxygen concentrations in estu-
aries was estimated from an equation predicting aerobic
degradation of carbohydrate (CH2O), where
O2 + CH2 O ! CO2 + H2 O ð6Þ
where O is oxygen, C is carbon and H is hydrogen.
Eq. (6) shows that for every mole (12 g) of C degraded, 1
molecule (32 g) of oxygen is required. In addition, the
reduced amino-N in organic matter may oxidise, so the
overall mass ratio is about 40 g of oxygen to 12 g of car-
bon. Using conversion ratios (by weight) for C:Chl of 25
(for summer) and 40 (for annual estimates) it is possible
to derive an empirical relationship for oxygen consumption
79
N losses: Microplankton
denitrification (%) loss rates (L, d1)
22–44% 1 (100%)
7–18% 1
2 0.3
(ConsO2) per unit chlorophyll. This can then be equated to
an acceptable threshold for carbon or chlorophyll biomass.
The overall equation tested here was
ConsO2 ðmg=lÞ ¼ ððmeasured Chl  C : ChlÞ  O : CÞ=1000
ð7Þ
These calculations are based on the assumption that an
estuary is a closed system, that all the available carbon is
broken down at the same time, and that this is all by aer-
obic respiration/degradation processes. These assumptions
give a very precautionary assessment of the likely impact of
chlorophyll or carbon on oxygen concentrations.
Using predicted rates of oxygen consumption it is possi-
ble to determine the chlorophyll concentration which may
result in detrimental oxygen depletion. This can then be
compared with measured oxygen levels in an estuary.
3. Results and discussion
3.1. Field data
Estuarine data were analysed in different salinity catego-
ries (0–10, 10–20 and 20–35), representing the upper, mid-
dle and lower reaches of estuaries. Physical and biological
processes occurring in these different salinity zones differ to
a greater or lesser extent, depending on the nature of the
estuary. Seasonal means and standard deviations for phys-
ical, chemical and biological data were calculated in each
salinity zone for each of the estuary categories (Fig. 2).
As expected, mean temperatures were highest in summer
in all estuary categories. Mean concentrations of total
nitrogen were generally highest in winter and in the upper
and middle reaches. Variability around mean values was
high for suspended particulate material (SPM) and chloro-
phyll concentrations. Nonetheless, seasonal and spatial
trends were apparent. Loads of SPM were generally highest
for estuaries in category A, and in the upper and middle
reaches of the estuaries. Mean chlorophyll concentrations
were generally highest in summer and in the upper reaches
of estuaries in categories A and B. The highest mean values
were observed in category B, where moderate light levels
and relatively long water residence times (weeks) promote
the development of the phytoplankton community. Data
were analysed to determine average SPMs in the different
estuary types proposed in this study. Average annual SPMs
in the three different salinity ranges (Fig. 3) indicate that
estuaries in category A and B are the most turbid, and that
80 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90

Mean Temp at sal 0 to 10 Mean Temp at sal 10 to 20 Mean Temp at sal 20 to 35

25 25 25
20 20 20
15 15 15
10 10 10
5 5 5
0 0 0
A B C A B C A B C

Mean TOxN at sal 0 to 10 Mean TOxN at sal 10 to 20 Mean TOxN at sal 20 to 35

1000 1000 1000
800 800 800
600 600 600
400 400 400
200 200 200
0 0 0
A B C A B C A B C

Mean SPM at sal 0 to 10 Mean SPM at sal 10-20 Mean SPM at sal 20-35
2000 2000 2000

1500 1500 1500

1000 1000 1000

500 500 500

0 0 0
A B C A B C A B C

Mean Chl at sal 0 to 10 Mean Chl at sal 10 to 20 Mean Chl at sal 20 to 35

200 200 200

150 150 150

100 100 100

50 50 50

0 0 0
A B C A B C
A B C

Fig. 2. Seasonal averages ( winter, spring, summer) for physical, chemical and biological data in the different types of estuaries. Error bars indicate
standard deviations. Data were analysed in different salinity (sal) categories, viz. 0–10, 10–20 and 20–35. Figure legends indicate temperature (Temp, C),
total oxidised nitrogen (TOxN, lM), suspended particulate material (SPM, mg l1), and chlorophyll (Chl, lg l1).

the variability in SPM is high throughout the salinity
ranges. Robust relationships could not be identified from
the available data, necessitating the development of a sim-
ple model to predict the biological response to nutrient
inputs.
Equating SPM values to the light regime was difficult,
particularly where values were high. Analysis of data from
coastal water (Fig. 4) showed a significant relationship
(r2 = 0.88) between SPM and the light attenuation coeffi-
cient (Kd) in these waters. Lower light levels were associ-
ated with values for SPM >35 mg l1 which, assuming a
linear relationship, is approximately equivalent to a Kd of
1 (m1). From the relationship between SPM and attenua-
tion coefficient (Kd) in coastal waters (y = 0.0213x + 0.183,
Fig. 4), Kd values were assigned to each of the estuarine
categories proposed in this study on the basis of the aver-
age SPM values in each category (Table 5). These Kd values
were used as default values in the model developed in this
study, but category C values were adjusted slightly to
reflect values considered to be more realistic of the light
regime.
In many UK estuaries information on light is not avail-
able. Secchi-disc depth may be used to indicate light
climate, as it provides a relative estimate of optical depth,

2000
0 to 10
10 to 20
20 to 35
1500
SPM (mg l-1)

1000

500

0
A B C

Fig. 3. Average annual values for suspended particulate material (SPM) in the different estuary types. Results are shown for the different salinity ranges
(0–10, 10–20, and 20–35). Error bars indicate standard deviation.
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90 81

1 higher SPM loads it is likely that the equation will not

0.9 remain linear so the Kd for a given SPM may be over/under
estimated. Furthermore, it is not only SPM that can affect
Light attenuation, Kd (m-1)

0.8
light attenuation but also concentrations of dissolved
0.7 organic material (DOM), chlorophyll, and gelbstoff, which
0.6 is more significant in estuarine systems. Here, we have
0.5 made the assumption that SPM is the dominant attenuator
0.4
of light and that the SPM spectrum is invariant between
estuaries, both of which are not likely to be true.
0.3 y = 0.02x + 0.18 The optical depth (Kd · h) provides a useful index
0.2 r 2 = 0.88 describing relative differences in sub-surface light regimes
0.1 in terms of a growth environment for algae between waters
0 of different transparency. It can be used to compare differ-
0 5 10 15 20 25 ent parts of an estuary or compare different estuaries in
Suspended Particulate Material (mg l-1) terms of photosynthetic potential and hence response to
nutrient input. In most UK estuaries the depth of the upper
Fig. 4. The relationship between SPM and attenuation coefficient (Kd,
m1) for coastal environments, using data obtained from cruises on RV mixed layer can usually be assumed to be the depth of the
Corystes (CEFAS, unpublished data). estuary, as most estuaries are well mixed. The exception
would be microtidal estuaries or lagoons, which may show
stratification.
Table 5 Annual nitrogen loads (Nedwell et al., 1999) were used
Mean values for SPM (mg l1) in the different estuary categories,
to predict annual net primary production in selected estu-
calculated using all available data. Estimates of Kd (m1) were obtained
from average SPM values using the relationship shown in Fig. 4 aries (Fig. 5), using the equation of Nixon et al. (1996). Pre-
dictions of primary production indicated that most of the
Estuary Mean SPM Std. Mean Kd Std. dev.
category (mg l1) dev. (m1) estuaries were eutrophic (301–500 g C m2 y1) or hyper-
trophic (>500 g C m2 y1). These values do not take
A 381.08 1045.63 8.30 22.46
B 224.39 387.87 4.96 8.45 account of light limitation of phytoplankton growth in
C 32.31 92.68 0.97 2.16 estuaries.

but is monitored infrequently. Routine measurements of 3.2. Model results and thresholds for nitrogen
SPM levels were therefore used here to represent light
availability in different estuary types, and their likely The screening model predicts potential maximum net
response to nutrient enrichment. There are, however, cer- primary production rates (g C m2 y1) in each of the estu-
tain caveats associated with this approach. The SPM values ary categories in response to concentrations of nitrogen
used to derive the relationship used in this study range (Fig. 6). Relative exchange rates and relative light levels,
from 0 to 25 mg l1, which is low for estuaries (particularly expressed as light attenuation coefficients, are the key driv-
Types A and B). Given the absence of light information at ers in this estuary specific model. Default values used in the
higher SPM values this is the best estimate at present. At model for these parameters are shown on Tables 4 and 5.
Primary Production (g C m-2 y-1)

1500
B

1000

B A
C C C C A
500
C C

0
t
ay
y

rn
ey

r
h

ar
es

i)
n

be
se

ac

yf
o

ve
w

w
am

pt

um
er

(D
ed

dd

Fo

Se
m
M
Th

aw

H
ey
ha

ov
M
ut

D
So

Fig. 5. Predictions of annual net primary production (PP, g C m2 y1) in UK estuaries from nitrogen loads, using the equation of Nixon et al. (1996):
log10PP = 0.442 log10 DIN + 2.332, where DIN = input of dissolved inorganic nitrogen (mol m2 y1). The dashed line represents a threshold (300 g C
m2 y1) for assessing eutrophic status (Nixon, 1995). Estuary categories are represented by A, B and C.
82 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90

700 the water column. More realistic estimates of production

1. Dyfi 2.8m
Production (g C m y )

C are likely to be obtained for these types of estuaries if the

-1

600 2. Mawddach 2.6m

depth of the euphotic zone is used in the model. For the
-2

3. Southampton water 3.12m

500
four initial test estuaries in categories A and B, higher esti-
400 mates of net primary production were obtained from the
300 B screening model if a euphotic zone depth of 0.1 m was used
3 instead of the mean depth of the estuary. Predictions in
200
1 A terms of g C m2 y1 were 36 for the Thames, 165 for
100 2
the Mersey, 30 for the Severn and 63 for the Humber.
0 While three of these estuaries remained oligotrophic, the
0 50 100 150 200 250 trophic status of the Mersey was changed to mesotrophic.
As a generic tool, the model indicates that estuaries with
1000
C 4. Medway 6.1m low light levels (such as the Humber and Severn) and mod-
Production (g C m y )
-1

800 5. Dart 4.9m erate light levels (such as the Thames and Mersey) are the
-2

6. Fowey 4.1m least likely to show a biological response to nutrient inputs.

600
400
6 10. Humber 5.9m
200 5
4
0 7
9 8
-200 10
-400
0 50 100
Equilibrium N concs (µM)
Fig. 6. Potential maximum net primary production rates (g C m2 y1) in
each of the estuary categories (lines A, B, C) in response to equilibrium
nitrogen concentrations (lM). (a) Model results based on an average
depth of 1 m for each estuary type, and (b) model results based on an
average depth of 5 m for each estuary type. Production rates predicted for
some UK estuaries (r) are also shown. Mean depths of each estuary (used
in the model) are indicated in the legend. For estuaries 1–3, predictions
were also made assuming mean depths of 1 m (grey symbols).
Fig. 6 also shows the model predictions of primary pro-
duction for the initial 10 test estuaries, for which basic data
were available (total areas, mean depths, mean water resi-
dence times, nitrogen loads). Predicted values per estuary
compared favourably with model predictions per category,
and indicated that most of these estuaries were oligo-
trophic, with four estuaries (the Dyfi, Southampton water,
Dart and Fowey) being identified as mesotrophic. All the
predictions of primary production, and particularly those
for estuaries in categories A and B, were considerably
lower than values predicted from the equation of Nixon
et al. (1996, see Fig. 5), which does not take account of
light limitation. For estuaries 1–3, predictions were also
made assuming mean euphotic zone depths of 1 m, to make
them more comparable with model results shown on
Fig. 6a. These yielded lower predictions of net primary pro-
duction, which agreed more closely with model results.
Mean depth of the estuary plays a critical role in deter-
mining phytoplankton production rates, especially in estu-
aries with low and moderate light levels. Where mean
depths of these estuaries are greater than 1 m, the model
predicts that there is no net production in the water column
(Fig. 6b). This is, however, likely to be unrealistic, as pri-
mary production may take place in the upper layers of
7. Thames 6.7m
8. Mersey 6.4m The model also indicates that estuaries with a good light
9. Severn 5.4m
regime (such as the Mawddach and Fowey) are likely to
be sensitive to nutrient enrichment, and to show similar
responses, mediated only by site-specific geomorphological
B
features.
A Predictions of primary production rates in different
150 200 250 estuarine categories may be used to set nitrogen and
chlorophyll thresholds for assessing the trophic status of
estuaries for which few data are available (Table 6). The
thresholds for eutrophic status are higher than existing
thresholds (Table 1), and need to be revised when sufficient
data are available to calibrate and validate the screening
model. The threshold values for assessing mesotrophic sta-
tus for category C estuaries (12–16 lM Nitrogen; 13–18 lg
Chl l1, Table 6) are comparable with CSTT and OSPAR
thresholds for eutrophic status (>12 and >15 lM Nitrogen,
>10 lg Chl l1, see Table 1). The thresholds for estuaries
with reduced light levels (Table 6) are considerably higher,
as ‘accelerated growth of algae’ is constrained by lack of
light.
3.3. Model results and thresholds for phosphorus
The screening model also predicts potential maximum
net primary production rates (g C m2 y1) in each of
the estuary categories in response to concentrations of
phosphorus (Fig. 7). The nutrient predicting the smallest
biomass increase, and therefore the lowest rate of primary
production, is considered to be the limiting one. Appli-
cation of the model to six test estuaries (Painting et al.,
2003), indicated that 5 out of the 6 estuaries (including
the Exe, below) were phosphorus-limited.
As for nitrogen, predicted primary production rates may
be used to set phosphorus and chlorophyll thresholds for
assessing the trophic status of estuaries (Table 6). Thres-
hold values for meso- and eutrophic status for category
C estuaries (0.5–2 lM) are comparable with OSPAR
thresholds for eutrophic status (>0.8 lM, Table 1).
Threshold values for predicted biomass are similar to
those for nitrogen (Table 6), due to the value used for
chlorophyll yield from phosphorus, viz. 30 mg Chl
(mmol DAIP)1. The use of higher conversion values, as
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90 83

Table 6
Proposed nutrient and chlorophyll thresholds for determining trophic status in each estuary category, using annual or daily (see text) net primary
production as a reference point. Thresholds are based on mean estuary depths of 1 m and 5 m. For estuaries in category A and B net production is negative
where depths are >1 m, resulting in thresholds of infinity () for nutrients. No thresholds (–) could be calculated for biomass. Biomass which accumulates
is due to growth in the top 1 m of the water column
Trophic status Reference point Proposed thresholds
Category A Category B Category C
2
Using primary production as a reference point Production (g C m ) 1 m, 5 m 1 m, 5 m 1 m, 5m
y1 OR d1
Nutrient concentrations
Dissolved inorganic nitrogen, lM Hypertrophic >500 >2.7 650,  313,  81, 61
Eutrophic >300 >1.7 390,  188,  49, 37
Mesotrophic >100 >0.6 130,  63,  16, 12
Dissolved inorganic phosphorus, lM Hypertrophic >500 >2.7 74,  12,  3, 2
Eutrophic >300 >1.7 14,  7,  2, 1
Mesotrophic >100 >0.6 5,  2,  0.6, 0.5
Phytoplankton chlorophyll biomass
Biomass (lg Chl l1) Hypertrophic >500 >2.7 715, – 344, – 89, 67
(from both DAIN and PO4) Eutrophic >300 >1.7 429, – 207, – 54, 40
Mesotrophic >100 >0.6 143, – 69, – 18, 13
O2 consumption
Using O2 consumption as a reference point
Phytoplankton chlorophyll biomass (lg Chl l1) Summer O2 consumptions = l mg l1 12 12 12
Annual 8 8 8
Dissolved inorganic nitrogen, lM Summer O2 consumptions = l mg l1 11 11 11
Annual 7.3 7.3 7.3

1000 recommended by the CSTT, would result in considerably

C lower thresholds for phosphorus concentrations (e.g., to
Production (g C m y )
-1

800 around 1 lM phosphorus at a chlorophyll yield of 50 to

-2

100 mg Chl (mmol DAIP)1 in category C estuaries with

600 an average depth of 1 m).
400 B
3.4. Applying the model on a seasonal basis
200
A
To apply the revised screening model to estuaries on a
0 seasonal basis, it is possible to use data from selected
0 2 4 6 8 10
months as inputs to the model. For example, for a classical
1000 spring phytoplankton bloom, equilibrium nutrient concen-
C
trations in late winter (February) or early spring (March–
Production (g C m y )
-1

800
April) may be used to predict the magnitude of the bloom
-2

600 and the potential maximum primary production rates. Cur-

400 rent assumptions in the model which are based on annual
estimates (e.g., mean 24-h surface PAR and ratios for phy-
200
toplankton C:Chl) also need to be adjusted to reflect the
0 relevant season. For assessment of trophic status, these val-
-200 B ues may be compared against the established thresholds.
A While these thresholds are relatively well established for
-400
0 2 4 6 8 10 winter nutrients and summer phytoplankton biomass, there
Equilibrium P concs (μM) are no comparable seasonal thresholds for primary
production.
Fig. 7. Potential maximum net primary production rate (g C m2 y1) in
Nixon’s threshold of 300 g C m2 y1 for eutrophic
each of the estuarine categories (A, B, C) in response to equilibrium
phosphorus concentrations (lM). (a) Model results based on an average waters may be adapted to apply a relative seasonal index
depth of 1 m for each estuary type, and (b) model results based on an for estuaries. A value of 300 g C m2 y1roughly approxi-
average depth of 5 m for each estuary type. mates to 1 g C m2 d1. This value is comparable with esti-
84 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90
mates from upwelling systems (Hutchings, 1992), which are
the most productive ecosystems in the world (Cushing,
1971), and are considered to be naturally eutrophic but
not suffering from eutrophication (Nixon, 1995). In UK
estuaries, phytoplankton growth takes place for approxi-
mately 3–6 months of the year. Nixon’s threshold for pri-
mary production for eutrophic water may therefore be
conservatively adapted (assuming a 6-month growing sea-
son) to a value of 1.7 g C m2 d1(see Table 6) for seasonal
growth in UK estuaries. Nixon’s thresholds for mesotro-
phic (0.6 g C m2 d1) and hypertrophic status (2.7 g C
m2 d1) may be adapted using the same simple assump-
tions (to 0.6 and 2.7 g C m2 d1 respectively, Table 6).
For estuaries there are limited data on annual primary
production estimates, making it difficult to apply Nixon’s
(1995) scale. There are also limited data on daily primary
production estimates, but they are more easily obtained.
A daily scale comparable to Nixon’s annual scale may
therefore provide a more useful standard for assessing the
impacts of nutrient enrichment.
3.5. Oxygen
For estuaries, the CSTT (1994, 1997) recommends that
a median concentration of 7 mg l1 be considered a safe
standard. Above this level, changes of <1 mg l1 are
acceptable. Below this level, more study is required. From
predicted rates of oxygen consumption at different chloro-
phyll concentrations (Fig. 8), the threshold chlorophyll
concentration above which a decrease in oxygen greater
than 1 mg l1 would occur would be 12 lg l1 for summer
values and 8 lg l1 for a total annual measurement (Table
6). Using the equations of Gowen et al. (1992, Edwards
et al., 2003) for chlorophyll yield from DAIN, this equates
5 tered during more detailed testing of the model on six
Oxygen consumption (mg l-1)
Y = 0.13X
4 and the availability of data, particularly field measure-
3 Y = 0.08X
2 issues applicable to all the test estuaries are summarised
1 Summer
Annual
0 data on nutrient loads (N only) were obtained from Lang-
0 10 20 30 40 50 60
Chl a (μg l-1)
Fig. 8. Predicted rates of oxygen consumption (mg l1) at different
concentrations of chlorophyll in an estuary (from Eq. (7), Methods).
Dotted lines indicate threshold concentrations (lg Chl l1) above which
oxygen consumption would exceed 1 mg l1. Threshold concentrations are
higher in summer (12 lg l1) than in winter (8 lg l1) due to lower
carbon:chlorophyll ratios. Thresholds are precautionary, due to assump-
tions that the estuary is a closed system, that all available carbon is broken
down at the same time, and by aerobic respiration/degradation processes.
to equilibrium nutrient concentration of 11 lM nitrogen
for summer, and 7.3 lM for annual averages (Table 6).
These threshold values represent a very precautionary
approach given the underlying assumptions (see methods).
This worst-case scenario is unlikely to occur in many
estuaries due to the effects of flushing and re-aeration in
response to (low) wind stress. Additional data on flushing
rates and BOD may enable a more accurate assessment
of oxygen utilisation to be made. The approach discussed
here is most applicable to areas of restricted exchange (such
as lagoons), and becomes less so as residence times and
flushing rates of estuaries increase.
Organic matter in an estuary may contribute directly
to eutrophication. The relative magnitude of the load of
inorganic versus organic nitrogen influences the balance
between autotrophic and heterotrophic metabolism.
Presumably because the relative magnitude of the load of
dissolved versus particulate organic matter influences the
residence time of the inputs. Particulate material is retained
by sinking and by processes operating at the turbidity
maximum. The carbon to nitrogen ratios of organic matter
remineralised by the benthic communities also influences
the balance between autotrophic and heterotrophic pro-
cesses in estuaries. Phytoplankton blooms are an example
of an autotrophic process and net oxygen uptake is an
example of a heterotrophic process. The impact of
increased inputs of organic particulate material in estuar-
ies has not been included in this study. However, impacts
are likely to be greatest where water residence times are
long.
3.6. Model performance
As shown above, 10 estuaries were selected for the initial
validation of the model, and predicted values for primary
production (Fig. 6) compared favourably with model pre-
dictions per category. Numerous difficulties were encoun-
estuaries, including issues of scale (temporal versus spatial),
ments of primary production rates and oxygen consump-
tion rates (Painting et al., 2003). Results of the model
validation are shown here for only the Exe estuary, and
below.
Data required to predict annual primary production for
the Exe estuary are summarised in Table 7. For 1996–2000,
70
ston et al. (2003). These were lower than the loads given by
Nedwell et al. (1999) for 1995/1996. The Exe is a bar-built
estuary and falls into category C in the model. Available
data show that water residence times in the estuary are
on the order of days, which is equivalent to a water
exchange rate of 0.3 d1in the model. Therefore the default
values were used in the model runs. Available data for
loads of suspended particulate material (SPM) indicate
that the Kd value for this estuary should be <0.6. A value
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90
Table 7
Data used to predict annual primary production for the Exe estuary using the simple screening model developed here and the model proposed by Nixon
et al. (1996)
Data input required
Area (km2)
Average depth (m)
Total N load
Total P load
Mean seawater conc.: Total N (lM)
Mean seawater conc.: Total P (lM)
Mean seawater conc.: Chl. (lg l1)
Mean water exchange rate (E, d1)
Mean phytoplankton losses (L, d1)
Estimated N losses (%)
Depth of upper mixed layer (m)
Mean 24-h total surface irradiance (W m2)
Mean light attenuation (Kd, m1)
Field measurements
Mean total N in estuary (lM)
Mean total P in estuary (lM)
Mean chlorophyll biomass in estuary (mg l1)
Mean oxygen conc. (mg l1)
The Exe is a bar-built, partly mixed, meso-tidal estuary with a relatively simple morphology (Rogers et al., 2003).
a
From Nedwell et al. (1999).
b
From Langston et al. (2003). Only l sewage plant included.
c
From Parr et al. (1999).
of 0.6 m1 was used in place of the default value in the
model. No data were available to test the assumptions
for phytoplankton losses, or mean 24-h total surface irradi-
ance. For nitrogen losses, a value (7%) was estimated from
residence time.
Model results were sensitive to the nutrient loads and
the mean concentrations of nutrients in coastal seawater.
Table 8 shows a summary of model results for five different
model runs. Results based on Nedwell’s nutrient data (runs
1 and 4) indicate that the Exe is a phosphorus-limited estu-
ary: predicted phytoplankton biomass and production
rates are lower for phosphorus loads than for nitrogen
loads. Using calculations based on phosphorus loads, equi-
librium nutrient concentrations were 2.04 lM for run 1.
Predictions for phytoplankton were 63.08 lg Chl l1,
674.9 g C m2 y1, and 1.9 g C m2 d1. The equation of
Nixon et al. (1996) predicts potential primary production
of 850.1 g C m2 y1. All of these values were higher than
those based on Langstone’s nutrient data (run 2). Model
results from runs 1 and 2 (Table 8) were comparable with
field observations for the Exe (Table 7), although they were
at the upper end of values for chlorophyll biomass. To
determine the trophic status of the Exe (Table 9), model
results based on phosphorus loads were compared with
thresholds for a 5 m deep estuary (Table 6). Assessments
of trophic status were the same when model results were
compared with thresholds for a 1 m estuary.
The third model run for the Exe was done using the
same inputs as for runs 1 and 2, except that upstream nutri-
85
The Exe
18.17
2.27
408.4 Mmol N y1a (=1118.9 kmol d1)
19,440 kg d1 (winter)b (=1388.6 kmol d1)
5011.2 kg d1 (summer)b (=357.9 kmol d1)
4,383,504 kg y1 (annual)b (=857.8 kmol d1)
7.75 Mmol P y1a (=21.23 kmol/d)
0.108 mg l1c (=7.71 lM)
0.010 mg l1c (=0.32 lM)
Default = 2
Residence time = 6 db, E = 0.3 d1 (Table 4)
Default = 0
±7% (Table 4)
Default = mean depth of estuary
Default = 150 W m2 (Table 3)
Mean SPM < 20 mg l1c From SPM, Kd = <0.6 (Fig. 4). Default = 0.97 (Table 6)
1–4 mg TIN l1b (=71–286 lM)
40–280 lg l1b (=1.3–9 lM)
Mean: 8–14 lg l1b
Max: 101 lg l1b
ca. 11.5 mg l1b
ent loads were assumed to be zero (and therefore losses due
to factors such as denitrification were zero). Model results
for nutrients and phytoplankton biomass were close to
the threshold indicating a transition from oligotrophic to
mesotrophic status. This suggests that the concentration
of nutrients and phytoplankton in seawater in coastal
water may have a significant impact on the estuary. These
inputs resulted in predicted primary production levels of
>100 g C m2 y1 (i.e., mesotrophic).
Runs 1 and 2 were therefore re-done, with nutrient con-
centrations and phytoplankton biomass in coastal seawater
set at the lower default values. The results of model run 4
(Table 8) are likely to be the most realistic for the Exe,
and were comparable with field observations (Table 7).
Equilibrium nutrient concentrations of 86 lM nitrogen
and 2 lM phosphorus (Table 8) were well within the ranges
of 71–286 lM nitrogen and 1.3–9 lM phosphorus (Table
7), but values of 55–97 lg l1 for chlorophyll biomass
(Table 8) were comparable with maximum values of up
to 101 lg l1 (Table 7). Potential primary production
(585 g C m2 y1, from phosphorus inputs, Table 8) was
lower than the value (850 g C m2 y1, Table 8) predicted
from the equation of Nixon et al. (1996), but still gave an
assessment of hypertrophic status (Table 9).
From model runs based on Nedwell’s nutrient loads
(runs 1 and 4), the maximum predicted chlorophyll
biomass exceeded 8 lg l1 and the oxygen consumption
thresholds proposed in Table 6, suggesting a strong poten-
tial for symptoms of eutrophication. Oxygen consumption
86 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90

Table 8
Exe estuary: summary of model results for five different model runs
Exe 1 2 3 4 5
Data input Nedwell Langstone No loads Nedwell Langstone
Total N load 408.4 Mmol y1 4,383,504 kg y1 zero 408.4 Mmol y1 4,383,504 kg y1
Total P load 7.75 Mmol y1 0 kg y1 zero 7.75 Mmol y1 0 kg y1
Model results
Total N load (kmol/d) 1118.90 857.83 0 1118.90 857.83
Total P load (kmol/d) 21.23 0 0 21.23 0
Seq (from N, lM) 91.81 72.18 7.71 86.10 66.47
Seq (from P, lM) 2.04 0.32 0.32 1.76 0.04
Xmax (from N, lg Chl l1) 102.99 81.40 10.48 96.71 75.12
Xmax (from P, lg Chl l1) 63.08 11.60 11.60 54.68 3.20
Growth rates (l d1) 0.32 0.32 0.32 0.32 0.32
Growth rates-losses (l d1) 0.02 0.02 0.02 0.02 0.02
Pmax (from N, g C m2 y1) 1101.82 870.89 112.13 1034.63 803.70
Pmax (from P, g C m2 y1) 674.86 124.10 124.10 584.99 34.24
Pmax (N, g C m2 d1) 3.02 2.39 0.31 2.83 2.20
Pmax (P, g C m2 d1) 1.85 0.34 0.34 1.60 0.09
Production from Nixon et al. (1996, g C m2 y1) 850.1 755.9 – 850.1 755.9
O2 Consumed (N, mg l1 d1) 13.73 10.85 1.40 12.89 10.02
O2 Consumed (P, mg l1 d1) 8.41 1.55 1.55 7.29 0.43
The source for data on nutrient loads is indicated at the top of each column (see Table 7). Oxygen consumption rates assume an annual C:Chl ratio of 40.
For explanation of abbreviations, see Eqs. (1)–(5) (methods) and Table 3. N = nitrogen, P = phosphorus.

Table 9
Comparison of the model results based on phosphorus (P) loads with threshold values for a 5 m deep estuary in category C (Table 6) to determine trophic
status of the Exe
Run 1 Run 2a Run 3 Run 4 Run 5a
Seq (from P) Hypertrophic Oligotrophica Oligotrophic Eutrophic Oligotrophica
Xmax (from P) Eutrophic Oligotrophica Oligotrophic Eutrophic Oligotrophica
Pmax (from P) Hypertrophic Mesotrophica Mesotrophic Hypertrophic Oligotrophica
Nixon’s Pmax (from N): Hypertrophic Hypertrophic No loads given Hypertrophic Hypertrophic
Assessments from results based on the equation of Nixon et al. (1996) using nitrogen (N) loads are also shown.
a
Assessments from runs 2 and 5 are unrealistic, as data on phosphorus loads were not available, and predictions are based on seawater inputs.

rates were calculated to be 7–8 mg l1 d1 (Table 8), which
exceeds the CSTT recommendation of <1 mg l1 d1.
The results from this (and other) test estuaries show that
the model is sensitive to the total nutrient inputs and to the
mean concentrations of nutrients in coastal seawater. Total
nutrient inputs need to be estimated as accurately as possi-
ble. The CSTT equations for calculating equilibrium nutri-
ent concentrations in estuaries need to be re-examined, or
the seawater concentrations of nutrients and phytoplank-
ton biomass need to be diluted before being incorporated
into the model.
In summary, the most realistic results for the Exe estu-
ary indicates that an overall assessment of trophic status
ranges from eutrophic to hypertrophic. Based on the nutri-
ent loads from Nedwell et al. (1999), a precautionary
approach would be to consider the estuary to be hypertro-
phic. Langston et al. (2003) concluded that the estuary
periodically exhibits symptoms of eutrophication, such as
elevated biological oxygen demand (BOD), the occurrence
of phytoplankton blooms, and toxic levels of ammonia.
Concerns regarding ecological implications for key habitats
and species resulted in the estuary being investigated as a
Sensitive Area (Eutrophic) during 2001. However, the area
may not be designated as a sensitive area, due to the
absence of strong evidence for water quality problems asso-
ciated with nutrient enrichment, thought to be largely due
to rapid flushing rates. During this study, available data
indicated that water residence times in the Exe are typical
of those for a bar-built estuary (i.e., days). Water residence
times of days were assumed to be equivalent to a water
exchange rate of 0.3 d1, which was assumed to allow
sufficient time for the development of microalgal com-
munities.
3.7. Seasonal analysis
Table 10 shows model results based on annual and sea-
sonal nitrogen loads obtained from Langston et al. (2003).
Considering that these loads may be underestimated (cf.
Nedwell’s loads), or overestimated due to phosphate limi-
tation, model results indicate relative trends. Relative
nutrient loads were highest in winter, as expected. High
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90 87

Table 10 Mmol y1 or as kmol d1. These loads had to be calculated

Exe estuary: summary of model results for seasonal model runs using N from the data sources which were available, which often
data from Langston et al. (2003), a Kd of 0.6 m1, and default values for
S0, X0, E and L
did not include all nutrient inputs. Discrepancies between
nutrient loads reported by Nedwell et al. (1999) and the
Annual Summer Winter
Environment Agency (EA) or the Countryside Council
Total N load (kmol/d) 857.83 357.94 1388.6 for Wales (CCW) indicate that not all calculations of nut-
Equilibrium N concentration (lM) 66.47 28.9 106.36
Xmax (lg Chl l1) 75.12 33.79 119.0
rient load include all anthropogenic sources (such as all
Growth rates (l d1) 0.32 0.68 0.25 sewage treatment works) or natural sources (such as atmo-
Growth rates-losses (l d1) 0.02 0.38 0.05 spheric loading). This procedure highlighted the need for
Pmax (g C m2 season1) 803.70 378.34 325.43 the establishment of detailed nutrient budgets for each
Production from Nixon et al. 755.9 – – estuary. Also, data which were available were not for the
(1996, g C m2 y1)
O2 consumed (mg l1 d1) 10.02 9.92 15.87
most recent years, and the model had to be tested using
data from the 1990s.
The assumed duration of seasons was six months (summer) and four
months (winter). Values used for mean 24-h total surface irradiance
It was relatively easy to use available data on nutrient
(W m2) were 150 (annual), 300 (summer) and 118 (winter). Oxygen loads to apply the models to the transitional waters of estu-
consumption rates assume C:Chl ratios of 40 for annual (and winter) data, arine systems. As mentioned above, transitional embay-
and 25 for summer. ments may differ considerably from transitional waters in
terms of their structure, and may therefore differ in terms
winter nutrient loads were reflected in the highest predic- of their hydro-dynamics and biological functioning. To
tion for phytoplankton biomass, and a high value for pro- apply the model to transitional embayments associated
duction. These results were not considered to be realistic, with transitional waters of estuaries would require infor-
and indicate that the equations describing the net yield of mation on nutrient loading to the transitional embayments
phytoplankton from nutrient inputs (from Gowen et al., themselves.
1992) may need to be adapted in order to carry out sea- Very few of the test estuaries had data on the site-spe-
sonal analyses. cific parameters required as inputs to the model, particu-
larly on the factors affecting the underwater optics. As a
3.8. Issues of scale result, default values had to be used for almost all the
parameters for most of the test estuaries. Similarly, very
In terms of spatial scales, the simplest option for testing few of the test estuaries had all the field data required for
the model is to apply it to the whole estuary. Some of the comparing model outputs with measurements in tidal
data required were initially easy to obtain for the whole waters. These include mean concentrations of total N and
estuary, for example the area (km2) and mean depth (m). total P in the tidal waters of the estuary, mean concentra-
Detailed examination of the data indicated complexities tions of dissolved oxygen, estimates of mean chlorophyll
in interpreting exactly how the data should be used (e.g., biomass, and estimates of daily or annual net phytoplank-
how to deal with transitional waters versus transitional ton primary production. As a result, the process of testing
embayments), and the usefulness of applying mean values and validating the model remains incomplete.
(e.g., depth, turbidity) to whole systems. However,
attempts to apply the model to various parts of an estuary 3.10. Validation of default values used in the model
highlighted different problems in obtaining and applying
the required data. For example, data on estuary dimen- Default values in the model are useful for the applica-
sions (area and mean depth) were not as easily obtained. tion of the model to estuaries where only limited data
Data on nutrient inputs or loads were difficult to apportion (e.g., nutrient loads) are available, and the estuary can be
between different parts of an estuary. assigned to one of the categories based on geomorphology
When the model is applied to different estuaries, latitude and relative light regimes. Where data are available, they
(as well as cloud cover) may need to be considered in order should be used to replace the default values. For all of
to obtain a more realistic estimate of mean light levels the test estuaries, only minimal data were available. It
available for phytoplankton growth. was therefore not possible to test all the default values
In terms of temporal scales, the simplest option for the developed for use in the model. The only parameter for
model is to apply it to annual estimates of nutrient load. which default values could be tested was the water
From the validation phase, it appeared that the model exchange rate, E, per day.
requires additional refinements to be applied on a seasonal Residence times from the recent typology study (Rogers
basis. et al., 2003) were used to obtain estimates of mean water
exchange rates for each of the test estuaries. For Milford-
3.9. Data availability Haven and the Stour-Orwell estuaries, default values for
E were not correct. For Milford-Haven, the default resi-
For all of the test estuaries, data on nutrient loads were dence time was ‘‘days’’ whereas the residence time calcu-
not readily available in the correct format, i.e., as lated by Rogers et al. (2003) was ‘‘weeks’’. Conversely,
88 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90
for the Stour-Orwell, the model default was ‘‘weeks’’
whereas observations indicate a residence time of ‘‘days’’.
As expected, the testing phase showed that different values
for E have a large impact on model outputs.
The development of this model highlighted the critical
need to incorporate light measurements in routine monitor-
ing programmes. This has been implemented and testing of
the model will be ongoing, as data become available. Pos-
sible incorporation of the model into the assessment tools
being developed under the Water Framework Directive will
facilitate extensive future testing of the model as a screen-
ing tool.
3.11. Development of an ecosystem approach for assessing
impacts of eutrophication in estuaries
An important contribution of this study towards improv-
ing our understanding of the impacts of eutrophication in
estuaries in England and Wales is the identification of dif-
ferent categories of response in terms of potential primary
production by the phytoplankton communities. These dif-
ferential responses are strongly influenced by the relative
retention times of water and the relative light regimes in
the different estuary categories. Once the simple screening
model developed here has been tested and validated, it
may contribute to future studies aimed at assessing the
response of different primary producers to nutrient enrich-
ment in our estuaries. Other factors may need to be consid-
ered, such as the relative extent of inter-tidal flats and
fringing salt marshes, substratum type and tidal dynamics.
Fig. 9. Conceptual diagram showing a hypothetical pattern of change in
the relative contribution by three groups of primary producers (phyto-
plankton, P; macroalgae, M; eelgrass or seagrass, S) in response to
changes in nutrient loading in shallow temperate estuaries with shorter
and longer residence times (from Valiela et al., 1997).
Valiela et al. (1997) proposed that water residence time
may play an important role in controlling the biological
response of different primary producers to nitrogen loading
(Fig. 9). They hypothesised that under high nutrient condi-
tions phytoplankton growth is likely to be limited when
water residence times are shorter, while macroalgae are
likely to become the dominant primary producers. Under
high nutrient conditions and longer residence times, phyto-
plankton are likely to become dominant, displacing the
eelgrasses and macroalgae. Eelgrasses are likely to contrib-
ute a larger proportion of the primary production when
nutrient conditions are low, especially in estuaries where
the water residence time is short.
The consequences of macroalgal blooms are more
indirect and extensive than the consequences of most
phytoplankton blooms, and tend to last much longer.
Mechanisms controlling rates of net production of macro-
algae are the same as for other primary producers, viz. tem-
perature, light, grazing and nutrients (Lowthian et al.,
1985; Valiela et al., 1997). In shallow temperate estuaries,
relatively small increases in nutrient loading favour macro-
algal blooms, which shade seagrasses and result in a sig-
nificant shift in the dominant primary producers from
seagrasses to macroalgal mats. In addition to water resi-
dence times, Valiela et al. (1997) demonstrated that the
response of macrophytes to nutrient loading may be signif-
icantly modified by the presence of fringing salt marsh, due
to reductions in nutrient loading through processes such as
denitrification or nutrient retention. These factors need to
be considered in ongoing and future studies aimed at
assessing the relative response of the different primary pro-
ducers in estuaries to nutrient enrichment.
4. Summary and conclusions
In this study, a number of approaches were adopted for
developing a generic tool for assessing the risks and
impacts of nutrient enrichment in estuaries. Primary pro-
duction by the phytoplankton community was considered
to be the key predictor for the effects of nutrient enrich-
ment. A simple screening model was developed to investi-
gate the growth of phytoplankton in different estuary
categories in response to their physico-chemical character-
istics, including relative light regimes. The model is sensi-
tive to the values used for all variables and parameters,
but relative water exchange rates (E) and relative light lev-
els, expressed as light attenuation (Kd), are the key drivers
influencing the biological response in the different estuary
types.
As a generic tool, the model indicates that estuaries with
low and moderate light levels are the least likely estuaries
to show a biological response to nutrient inputs. Estuaries
with good light regimes are sensitive to nutrient enrich-
ment, and are likely to show similar responses, mediated
by site-specific geomorphological and hydro-dynamic fea-
tures (such as mean water depth and water residence times)
which limit or control phytoplankton growth. For estuaries
 S.J. Painting et al. / Marine Pollution Bulletin 55 (2007) 74–90
where data are available, the model may be used to obtain
reliable predictions of the magnitude of primary produc-
tion. Nixon’s (1995) scale for assessing trophic status needs
to be validated for estuaries, but is useful for describing the
relative trophic status of estuaries in England and Wales,
and for observing changes in trophic status which are likely
to have an impact on features of conservation areas (e.g.,
under the Habitats Directive). Estuaries identified as being
eutrophic may not show any signs of eutrophication. Attri-
butes considered to be symptoms of negative impacts of
nutrient enrichment on estuarine ecosystems include the
development of hypoxic (and anoxic) conditions, blooms
of toxic algae, increased growth of epiphytic algae, the loss
of submerged vegetation, and the growth of macroalgae.
Standards have been set here on the basis of likely detri-
ment to the oxygen regime, but there is a need to develop
this approach further through application and research.
Linkages to other recent studies for the Environment
Agency on macroalgal blooms, and developments under
the Water Framework Directive will contribute towards
the setting of additional standards.
Initial validation of the model indicates that it provides
a useful tool for assessing the risks and impacts of nutrient
enrichment in estuaries in England and Wales. Robust
assessments of trophic status are dependent upon reliable
estimates of nutrient loading and improved availability of
data linking nutrient loading with biological effect in the
different estuary types (e.g., light, and production rates of
primary producers). Equations in the model need to be
improved to account for dilution of inputs of nutrients
and phytoplankton from coastal waters, particularly for
estuaries dominated by freshwater inputs, and to carry
out seasonal analyses of the biological response to nutrient
inputs.
Acknowledgements
This work was supported by contract C1706, which was
funded by the Environment Agency, English Nature and
the Countryside Council for Wales. Comments on an
earlier version of the manuscript by Mike Best and ano-
nymous reviewers were greatly appreciated.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at doi:10.1016/j.marpolbul.
2006.08.020.
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