Aquaculture 212 (2002) 191 – 211

www.elsevier.com/locate/aqua-online

Empirical mass balance models calibrated for

freshwater fish farm emissions
Torbjörn Johansson *, Lennart Nordvarg
Department of Earth Sciences, Uppsala University, Villavägen 16, SE-752 36 Uppsala, Sweden

Received 16 December 2000; received in revised form 28 December 2001; accepted 31 December 2001

Abstract

Existing mass balance models for phosphorus were tested for fish farm emissions in eight
Northern and Central European lakes. These traditional models overestimated the total phosphorus
concentration in these lakes by, on average, a factor of two. Data from the eight lakes were therefore
used to calibrate emission specific models based on the Vollenweider and Dillon – Rigler structures.
With this approach, it was possible to improve the accuracy of the models and to eliminate
systematic errors. The new models gave r2 values ranging between 0.90 and 0.92. It was not possible
to detect any differences in phosphorus – chlorophyll relationships between lakes with or without fish
farm emissions. Neither were there any significant differences between measurements in farm lakes
and results obtained from phosphorus – chlorophyll models found in the scientific literature. In the
future, however, data from more lakes will be needed to further test the new models and to
investigate other effect parameters, e.g. phytoplankton biomass and hypolimnetic oxygen
concentrations.
D 2002 Elsevier Science B.V. All rights reserved.

Keywords: Fish farming; Eutrophication; Models; Phosphorus; Chlorophyll; Lakes

1. Introduction

Aquaculture is an industry which may cause negative effects on the environment,

especially in lakes, which are usually more sensitive to point emissions than marine lo-
cations, due to the generally much slower water exchange in lakes (Persson et al., 1994). To
allow for fish farms in lakes and at the same time protect the environment, it is essential to
develop tools to estimate the environmental impact from fish farms (e.g. Gowen, 1994;

*
Corresponding author. Tel.: +46-1847-12415; fax: +46-1847-12737.
E-mail address: torbjorn.johansson@geo.uu.se (T. Johansson).

0044-8486/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 0 4 4 - 8 4 8 6 ( 0 2 ) 0 0 0 1 3 - 3
192 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

Beveridge, 1996). However, most studies have focused on the amounts and characteristics of
emissions (Penczak et al., 1982; Beveridge et al., 1991; Axler et al., 1993; Phillips et al.,
1993; Cripps, 1995; Gavine et al., 1995; Massik and Costello, 1995; Garzia-Ruiz and Hall,
1996), or on the local effects in sediments underneath fish cages (Enell and Löf, 1983;
Turrell and Munro, 1988; Holby and Hall, 1991; Maloney et al., 1992; Ye et al., 1991;
Silvert, 1992; Kelly, 1993; Findlay and Watling, 1994; Gowen et al., 1994; Silvert, 1994;
Holmer and Kristensen, 1995).
As a consequence, the few farm specific models that have been suggested for estimating
the effects of farm emissions on a whole lake scale (Beveridge, 1996; Håkanson et al., 1998)
have not been statistically tested, and are therefore seldom used in practical lake manage-
ment. Instead, eutrophication effects of freshwater fish farms are usually estimated from
traditional total phosphorus (TP) mass balance models (Kirchner and Dillon, 1975;
Vollenweider, 1975; OECD, 1982; etc.). These traditional models are not explicitly
calibrated for any particular type of emission. In reality, though, they are strongly influenced
by the most commonly occurring emission types, e.g. sewage and runoff from urban and
agricultural areas. Other types of emissions, e.g. fish farm emissions, may behave differ-
ently, and in such cases model predictions and uncertainty estimates would be biased.
Beveridge (1996) suggested that effects of fish farm emissions on TP were approximately
45– 55% of the values predicted from the Dillon– Rigler model (Kirchner and Dillon,
1975). Beveridge based his estimates on observed phosphorus deposition underneath the
cages and the assumption that the retention of other phosphorus fractions could be estimated
by the Dillon– Rigler model. This estimate was not, however, tested against empirical data
on TP.
Considering the complexity of phosphorus circulation in lakes, it is necessary to
measure the actual changes in TP related to fish farm emissions in order to investigate the
usefulness of the traditional models and, if necessary, calibrate farm specific models.
Unfortunately, the data requirements for complete mass balance calculations based on such
measurements are rarely fulfilled, and such calculations have only been done for one or a
few lakes at a time (Stirling and Dey, 1990; Persson, 1991; Håkanson et al., 1998).
According to Persson (1991) and Stirling and Dey (1990), the fish farm effects were in
rough agreement with predicted values from OECD and Dillon –Rigler models. Håkanson
et al. (1998), on the other hand, found that the Vollenweider model overestimated the
effects considerably. As a consequence, they suggested a farm specific calibration by using
a fixed extra elimination factor, much in the same way as suggested by Beveridge (1996)
for the Dillon– Rigler model. However, due to the small number of lakes in each of these
studies, the models were never tested statistically for farm emissions. Another problem,
besides the small number of investigated lakes, is the deviations from steady state in lakes
where measurements were made shortly after farm introduction (Cornel and Whoriskey,
1993; Yokom et al., 1997; Håkanson et al., 1998). In some fish farming lakes, it may also
be difficult to distinguish farm effects from effects of changes in other human activities
(Kelly, 1995). As a conclusion, the adequacy of existing traditional models for fish farm
emissions has not been statistically tested and no farm-specific calibrations have been
made.
The main aim of this investigation was to develop phosphorus mass balance models
specifically calibrated for freshwater fish farm emission, and to test whether the relation
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 193

between farm-emitted phosphorus and effects on chlorophyll-a concentrations (Chl-a)

differs from general empirical relationships. The phosphorus models are intended to be
used as routine tools in environmental impact assessments. They must therefore be simple
and inexpensive to use. A secondary aim was to investigate the sedimentation character-
istics of farm emitted phosphorus, especially the relationship between net sedimentation
rate and water retention time.

2. Materials and methods

2.1. Water sampling and analysis

The models developed within this project are based on data from eight lakes, of which
six are Swedish (Fig. 1), one Polish (Szczytno Male; Korzeniewski et al., 1985) and one
Scottish (Loch Fad; Stirling and Dey, 1990). Data for the Swedish lakes were provided by
local authorities or collected from the scientific literature (Enell and Löf, 1983; Persson,
1991). Some morphometrical and hydrological data emanate from the Swedish meteoro-
logical and hydrological institute (SMHI, 1993, 1994a,b, 1996a,b, 1998). We also carried
out extensive field studies in three of the Swedish lakes between May and October 1999
(Lakes Långvattnet, Framsjön and Gissjön). Lake water was sampled twice a month from
a total of seven sampling locations in the farm lakes and four reference locations. Samples
were taken at 2.5-m intervals in the epilimnion and from two different depths in the
hypolimnion. The water samples were kept dark and cold and were filtered through
Whatman GF/C glass microfibre filters within 24 h after sampling. Filters, filtered water
and unfiltered water were then frozen until analysis. Water and filters were analysed within
1 month for total phosphorus, dissolved phosphorus, total nitrogen, Chl-a, Chl-b, Chl-c,
phaeophytin, total suspended matter (SPM), suspended inorganic (SPIM) and organic
(SPOM) matter. Total and dissolved phosphorus was analysed on unfiltered and filtered
water, respectively, according to the Swedish standard method SS 02 81 27. Total nitrogen
was analysed on unfiltered water by an accredited laboratory according to the Swedish
standard method SIS 02 81 31. For the TN analyses, water samples from each month were
pooled to produce monthly average samples for each sampling station and water layer. The
chlorophyll was extracted with acetone and analysed with a spectrophotometer (Hitachi U-
2000) at the following wave lengths: 750, 665, 645, 630 and 480 (Parsons and Strickland,
1963; Lorenzen, 1967; Strickland and Parssons, 1968), Swedish standard method SS 02 81
46. The filters used for suspended matter analysis were dried at 105 jC for 6 h and re-
weighed to determine the SPM concentration . The inorganic fraction (SPIM) was
determined after heating the filters at 550 jC for 2 h. Temperature and oxygen
concentrations were measured in situ with 2.5– 5-m intervals from the surface to the
bottom, using a YSIR 58 dissolved oxygen meter.
Morphometrical, hydrological, water chemical and farm production data for all lakes
are given in Table 1. When possible, total phosphorus concentrations were calculated as
epilimnetic mean values for the production period (May – October), in accordance with
Swedish EPA recommendations (Persson, 1999). Chl-a concentrations are also given as
epilimnetic mean values for the production period and as seasonal maximum values.
194 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

Fig. 1. Map of the Swedish lakes included in this study.

Table 1
Lake specific data on hydrology, morphometry, water chemistry and farm production
Framsjön Gissjön Loch Fad Långsjön Långvattnet Szczytno Male Skärsjön Västra Silen Sarvtjärn Southern Bullaren
X 667,307 693,243 Scotland 671,974 664,030 Poland 633,344 656,961 664,954 652,705

T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

Y 138,723 152,189 152,544 147,050 130,068 128,876 143,405 125,521
A (km2) 1.8 3.1 0.71 0.16 1 0.332 3.1 48 0.09 8.28
Dm (m) 7.2 14 5 2.1 7.1 3.6 9.4 15 8.1 10.1
Dmax (m) 25 35 6.2 24 8.5 22.5 – 25 26
V 13 44 3.6 0.34 7.4 1.2 29 720 0.73 83.6
ADA 214 292 3.3 24.1 14.5 733 0.36 199
Q 79 106 7.4 1.12 9.2 168 6.4 303 0.19 94
qs 11.7 11.5 10.8 12.1 14 13.1 17.0 15
T 0.17 0.41 0.48 0.3 0.8 0.007 4.55 2.4 3.77 0.89

DTPin 5.6 1.9 508 43.5 27 3.9 70 5.7 61 –

DTP 2.5 0.9 100 5.5 16 3.1 8 1 1.65 –
TP 10 8.3 112 13 24 85 14 6.2 13 27
Chl-a (mean) 4.6 2.2 73 7 12 13 – 2.4 5 4.6
Chl-a (max) 8.8 5.2 157 9 22 – 6.1 – 7 8

Prod 68 29 200 – 37 26 33 255 – –

Pfarm 442 201 3757 49 248 650 448 1727 – –
Farming period 1982 – 1987 – 1976 – 1987 – 1989 1978 – 1979 – 1978 – 1985 1986 – 1987 – 1989 1982 – 1994
Data availability 1990 – 1999 1989 – 1999 1981 1986 – 1989 1996, 1999 1981 – 1982 1982 – 1999 1990 – 1996 1986 – 1989 1983 – 1998
X/Y = Lat/long coordinates according to the Swedish national coordinate system; A = lake area (km2); Dm = mean depth (m); Dmax = maximum depth (m); V = lake volume
(mm3); ADA = area of drainage area (km2); Q = annual water flow (106 m3 year
1); qs = specific runoff (l s
1 km
2); T = theoretical water turnover time (year) = V/Q;
TPin = inflow concentration for total phosphorus to the lake (mg/m3); TP = total phosphorus concentration in epilimnion (mg/m3); DTP and DTPin = effect of farm
emissions on TP and TPin (mg/m3); Chl-a (mean) = seasonal mean concentration of chlorophyll-a in epilimnion (mg/m3); Chl-a (max) = seasonal maximum concentration
of chlorophyll-a in epilimnion (mg/m3); Prod = annual farm production (ton * year
1); Pfarm = annual phosphorus emissions from the fish farm (kg/year).

195
196 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

2.2. Data requirements

Since the purpose of this work is to develop steady-state models, the lakes that are
included must have had enough time after farm establishment to equilibrate to the new
load. For obvious reasons this time must be longer than the theoretical retention time of
emitted phosphorus, which depends on the sedimentation rate of the emissions (KT) and the
theoretical water retention time, T (OECD, 1982). Most of the effects are probably
manifested after one retention time, although this is probably insufficient for a true steady
state to develop (see OECD, 1982). The response time of sediments and biota can be
considerably longer, and it may require several renewal times before the steady-state effects
can be estimated. The emissions must also be large enough for the effects to be measurable.
For the analyses of the relation between TP and Chl-a concentrations, it is not necessary
for the phosphorus concentration in the lake to be equilibrated. Also, only some of these
analyses require data on farm emissions (DTPin). For this reason, two more lakes were
included, Lake Sarvtjärn (Håkanson et al., 1998), which was not equilibrated at the time of
the sampling, and Lake Southern Bullaren (Håkanson and Carlsson, 1998; Johansson et
al., 1998), where the data on farm production are uncertain.
To calibrate farm-specific models, it is necessary to have data on farm emissions and TP
in the lakes before and after farm establishment, or some other measure of the reference TP.
When possible, reference values of TP (TPref), i.e. expected TP without farm emissions,
were estimated from data collected before farm establishment (Lake Skärsjön, Lake
Långsjön and Lake Sarvtjärn). Reference values were estimated from a database of
undisturbed reference lakes in the respective regions of Lake Långvattnet, Lake Framsjön
and Lake Gissjön, together with data from undisturbed upstream lakes or inflowing water
and water colour. Water colour has been shown to affect natural TP concentration (Meili,
1992), and it has been suggested that TPref can be estimated from colour or absorbance at
420 nm of filtered water, when other data are not available (Persson, 1999). Therefore, it
was important to estimate TPref from lakes with similar colour as the farm lakes. Since we
had data from undisturbed lakes with similar characteristics as the farm lakes, we mainly
used color and absorbance to test the adequacy of the chosen reference lakes, instead of
predicting TPref directly from the absorbance– TP relationship presented in Persson (1999).
There was a very strong relationship between TP and absorbance in the reference lakes
close to Lake Framsjön. Lake Framsjön receives approximately 90% of its water directly
from Lake Knon, and the water colour in these two lakes are nearly identical. Data from
the northern part of Lake Knon is available for 1996 –1997 and we measured TP in the
summer of 1999 in the inflow to Lake Framsjön. We believe that those data give a good
estimate of TPref for Lake Framsjön. Most of the water entering Lake Långvattnet
emanates from Lake Kloten, whose drainage area makes up 78% of the drainage area
of Lake Långvattnet. TP data was available from the central parts of Lake Kloten for the
period 1993 – 1998, and we sampled water from the outflow in 1999. The average surface
TP concentration in Lake Kloten was 6 Ag/l, but this lake is clearer than Lake Långvattnet.
Based on colour and TP data from Lake Kloten and other undisturbed lakes in the region,
TPref for Lake Långvattnet was estimated to 8 Ag/l. We analysed water samples from Lake
Gissjön and its two major inflows during 1999. Such data were also available for 1989.
For 1993 and 1996 – 1998, TP data from September for Lake Gissjön were available. The
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 197

average TP in Lake Gissjön and the flow weighted average for the inflows were nearly
equal. However, streams are less suitable as reference locations, since some of the
phosphorus is likely to settle in the lake. TPref in Lake Gissjön may therefore be lower
than the inflow concentration. The colour – TP relationship in undisturbed lakes in the
region showed larger variation than in the other regions, and estimated reference values
from this relationship is more uncertain compared to the other two lakes. However,
although variable, the relationship does not depart systematically from the equation
suggested by Persson (1999). This equation estimates a TPref of 7.4 Ag/l for Lake Gissjön.
Although this estimate is uncertain it should be unbiased, which is important for the
statistical analysis. The major part of the inflowing water to Lake Västra Silen comes
directly from Lake Östra Silen. The colours of these two lakes are practically identical and
it was assumed that the inflowing water from Lake Östra Silen could be used as an
estimate of TPref. In Lake Szczytno Male, data from the sampling station immediately
upstream of the lake was used as reference. The major inflow totally dominates the
drainage area of this lake. For Loch Fad, data from Stirling and Dey (1990) were used.
They estimated the background concentrations from watershed characteristics. TP in Loch
Fad was estimated from measured phosphate concentrations, using relations between TP
and phosphate measured earlier in the same lake (Stirling and Dey, 1990).

2.3. Test of existing models against fish farm data

Two different model structures were tested against fish farm data. The Vollenweider type
models (Eqs. (1a – b) and (2a – d)) calculate retention as a function of the theoretical water
retention time (T), while in the tested calibration of the Dillon –Rigler model (Eq. (3)),
retention is a function of areal water loading ( q = Dm/T, Eq. (4); Kirchner and Dillon, 1975).
The tested Vollenweider type models were the original calibration (Vollenweider, 1975;
Eq. (1b) and different calibrations from OECD (1982) (Eqs. (2a) – (2d)). The OECD
calibration for shallow lakes and reservoirs (Eq. (2c)) was used for Loch Fad and Lake
Szczytno Male, and the calibration for Nordic lakes (Eq. (2d)) was used for the Swedish
lakes, which are stratified during summer.
The Vollenweider structure:

DTPin DTPin
DTP ¼ c ð1aÞ
ð1 þ KT *T Þ ð1 þ a*T b Þ

(Vollenweider, 1975):

a ¼ 1; b ¼ 0:5 ð1bÞ

(OECD, 1982):
!b
DTPin
DTP ¼ a* pffiffiffiffi ð2aÞ
ð1 þ T Þ
198 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

OECD combined dataset:

a ¼ 1:55; b ¼ 0:82 ð2bÞ
OECD Shallow lakes and reservoirs:
a ¼ 1:02; b ¼ 0:88 ð2cÞ
OECD Nordic lakes:
a ¼ 1:12; b ¼ 0:92 ð2dÞ
(Dillon and Rigler, 1974)
DTP ¼ DTPin *ð1
RÞ ð3Þ

where:

KT = net sedimentation rate (year
1);

R = retention rate (dimensionless);
DTP = effect of fish farm emissions on total phosphorus concentration (Ag/l);
DTPin = farm emissions of phosphorus, described as the effect on inflow concentration
(Ag/l).

For the Dillon– Rigler model, the following calibration was used for the retention rate
(Kirchner and Dillon, 1975):
RKD ¼ 0:426*e
0:271*Dm =T þ 0:574*e
0:00949*Dm =T ð4Þ
Linear regression analysis was used to estimate the correlation between modeled and
empirical values and paired t-test to test for differences between general calibrations of
these models and measured effects of fish farm effluents.

2.4. Fish farm-specific model calibrations

Fish farm data were used to calibrate the Vollenweider and Dillon– Rigler type models
using several different algorithms and two different target variables, DTP and DTP/DTPin.
For the Vollenweider models, the two algorithms in Eqs. (1a) and (2a) were used, where a
and b are the parameters to be calibrated. Two similar algorithms were used for the
Dillon – Rigler models. The models only estimate the contribution of fish farm emissions
to TP, which is possible assuming that the effects of different emissions are additive. The
basic model structure is also described in Fig. 2. DTP models were calibrated using log10
transformed values and the logistic transformation (Eq. (5)) was used to normalise the
DTP/DTPin data. DTP was fitted to models 1, 2 and 4 in Table 3 using linear regression,
and nonlinear numeric regression was used for all other calibrations.
The logistic transformation:
 x 
logitðxÞ ¼ ln ð5Þ
1
x
To test the stability of the new model calibrations, cross validation was performed for two
of the models. One data point at a time was excluded from the data set and the models were
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 199

Fig. 2. Illustration of the basic principle of the mass balance models, which are based on the Vollenweider structure.
The same basic structure applies for models based on the Dillon – Rigler model. Pfarm = annual farm emissions of
phosphorus (kg year
1). TPref = Steady-state TP concentration in the lake without farm emissions (mg m3).
KTfarm = Net sedimentation rate of phosphorus emitted from the fish farm (year
1). KTref = Net sedimentation
rate of phosphorus from all other sources (year
1). All other abbreviations according to Table 1.

fitted to the remaining data set. Results are given as the observed variation of the calibration
parameters a and b, and as the ability of these eight model calibrations to predict the
excluded data points, described by the correlation coefficient (r2) and standard error (s.e.) for
the regression between predicted and observed log(DTP). Although this is not a true
validation, it will give information on the stability of the models and on the influence of each
data point for the results.

2.5. Phosphorus– chlorophyll-a relationships

It is possible that the relation between TP in lake water and phytoplankton biomass is
different in lakes dominated by fish farm emissions, compared to other lakes. The reason
could be, e.g. the different seasonal pattern of farm emissions may affect the primary
production differently or that the bioavailability of farm emissions may be different from

Table 2
Test of differences between measured and predicted DTP caused by fish farm emissions, using t-test on log10
transformed values
Model Mean difference P n
OECD mixed 0.232 0.025 8
Kirchner – Dillon 0.203 0.024 8
Vollenweider 0.288 0.014 8
OECD mixed denotes a mixture of different OECD calibrations. The OECD models for shallow lakes and
reservoirs were used for Loch Fad and Lake Szczytno Male and the OECD model for Nordic lakes for all other
lakes.
200 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

Fig. 3. Measured effects of fish farm emissions on total phosphorus concentration (DTP) compared to (A) the
farm load (DTPin) and (B) to predictions using the OECD model (Eqs. (2c) and (2d)).
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 201

Table 3
Farm emission specific calibrations of TP models
(a) Regressions on log DTP
Model Algorithm a b r 2 (log10) s.e. (log10)
b
1 DTP = a*DTPin 0.56 0.77 0.84 0.287
2 DTP = a*(DTPin/(1 + MT))b 0.77 0.82 0.90 0.230
3 DTP = DTPin/(1 + a*T b) 3.3 0.41 0.91 0.258
4 DTP = a*(DTPin*(1
RKD))b 0.78 0.90 0.92 0.200

(b) Regressions on logit DTP/DTPin

Model Algorithm a b r 2 (logit) r 2 (log10) s.e. (log10)
b
5 DTP/DTPin = 1/(1 + a*T ) 3.06 0.47 0.55 0.91 0.261
6 DTP/DTPin = a*(1
RKD) 0.723 – 0.67 0.92 0.226
For models in Table 4b, r2 and s.e. for log DTP are given for all calibrations, to make it possible to compare the
models.

that of the other phosphorus sources. To test this possibility, empirical data on chlorophyll-
a concentrations (Chl-a) in farm lakes were compared to TP – Chl-a relationships from
other investigations (Dillon and Rigler, 1974; OECD, 1982; Meeuwig and Peters, 1996).
Linear regression and paired t-test were used to compare the predictions with measured
Chl-a. This was also done for a set of 17 reference lakes without anthropogenic phosphorus
sources, situated close to Lakes Framsjön, Gissjön, S Bullaren, Långvattnet and Västra
Silen. We used total concentrations, TP and Chl-a, instead of estimated farm effects, DTP
and DChl, since most of the lakes with fish farms lacked data on the reference value for
Chl-a.

Table 4
Comparison of DTP predicted from the different models
Framsjön Gissjön Loch Långsjön Långvattnet Szczytno Västra Skärsjön
Fad Male Silen
T (years) 0.17 0.41 0.48 0.3 0.8 0.007 2.4 4.55
DTPin 5.6 1.9 508 43.5 27 3.9 5.7 70
DTP empirical 2.5 0.9 100 5.5 16 3.1 1.0 8.1
TP empirical 4.0 1.2 300 28 14 3.6 2.2 22
DTP Vollenweider 3.4 1.1 231 17 12 3.9 2.2 14
DTP K – D 4.8 1.7 167 24 14 4.4 3.0 20
DTP OECD 4.0 1.3 213 24 13 3.6 2.3 19
DTP OECD N 154 3.1
DTP OECD shallow 4.0 1.3 154 24 13 3.1 2.3 19

Farm specific models for DTP

1 2.1 0.9 68 10.2 7.1 1.6 2.1 15
2 2.4 0.9 83 11.9 6.8 2.2 1.5 9.8
3 2.2 0.6 147 14.4 6.7 2.7 1.0 9.8
4 2.4 0.9 105 10.2 7.1 2.6 1.6 8.1
5 2.4 0.6 160 15.9 7.2 3.0 1.0 9.7
6 2.5 0.8 167 12.5 8.5 2.8 1.6 9.8
All values except for the water retention time (T; years) are expressed as Ag/l.
202 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

Fig. 4. Relation between phosphorus elimination and T for fish farm emissions. From this regression, the net
sedimentation rate for farm emitted phosphorus is calculated as: KTfarm = 3.06 * T
0.53 c 3/MT (year
1).

Fig. 5. Calibration results and 95% confidence intervals for model 4 (Table 3), the model with the lowest estimated
uncertainty.
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 203

3. Results

3.1. Existing phosphorus models

Empirical DTP was compared to predictions using the existing traditional models (Table
2; Fig. 3B). The correlations between measured and predicted values were stronger than
between measured values and phosphorus load (DTPin; Fig. 3A), indicating that the model
algorithms explain some of the lakes variation in phosphorus retention. However, all models
overestimated DTP significantly (Table 2, Fig. 3B).

3.2. Fish farm-specific phosphorus model calibrations

The farm-specific model calibrations are given in Table 3 and predicted DTP for both
traditional and farm-specific models are compiled in Table 4. The differences among the
models were small. However, DTP predicted from the farm-specific models are approx-
imately 50% lower than the predictions from existing traditional models, i.e. traditional
models gave, on average, two times higher DTP. The estimated net sedimentation rates (KT)
are approximately 3– 4 times higher than the KT in the original Vollenweider model (model
6 in Table 3; Fig. 4). The uncertainty of the models is described in Table 6 as the standard
error of the regression (s.e.), and, as an example, the confidence intervals of model 4 from
Table 3 are described in Fig. 5.
The results of the cross validations of models 2 and 5 from Table 3 are given in Table 5.
Exclusion of single data points had little effect on the regression coefficients. For model 2,

Table 5
Results of stability tests of models 2 and 5 (Table 3)
Excluded lake Observed DTP Model 2 Model 5
a b Predicted DTP a b Predicted DTP
Gissjön 0.9 0.76 0.83 0.9 3.34 0.47 0.6
Framsjön 2.5 0.76 0.83 2.4 3.09 0.46 2.4
V Silen 1.0 0.89 0.79 1.7 3.05 0.47 1.0
LåS 16.0 0.71 0.81 6.1 3.90 0.51 6.0
Skärsjön 8.1 0.78 0.83 10.4 2.75 0.46 10.7
Långvattnet CaHg 5.4 0.79 0.87 14.3 3.05 0.41 15.2
Loch Fad 100 0.86 0.76 63.4 2.90 0.45 164
Szczytno Male 3.1 0.70 0.84 2.1 2.36 0.48 3.2

Min 0.70 0.76 2.36 0.41

Max 0.89 0.87 3.90 0.51
Mean value 0.78 0.82 3.05 0.46

r2 (log DTP) 0.85 0.89

s.e. (log DTP) 0.285 0.281
One lake at a time was excluded and the models recalibrated using the remaining lakes. These recalibrated models
were then used to predict the effects in the excluded lakes (predicted DTP), which were compared to observed
DTP. The results are shown as correlation coefficients (r2) and standard errors (s.e.) for the regressions between
predicted and observed log(DTP).
204 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

Table 6
Test of difference between measured Chl-a in farm lakes and predictions with existing TP – Chl-a models and
with measured TP – Chl-a relationships in reference lakes close to the Swedish fish farm lakes (reference lake
model)
Model Mean difference P n
OECD annual 0.15 0.082 9
Willén 0.01 0.91 9
M–P 0.10 0.24 9
K–D 0.10 0.38 9
Reference lake model
0.13 0.12 9
The differences were tested with paired t-test on log chl-a.

the coefficient a ranged between 0.70 and 0.89 and b between 0.76 and 0.87. Comparison
of observed and predicted logDTP for the excluded lakes resulted in a slight increase in
regression error (s.e.) from 0.230 to 0.284 compared to the calibration where all lakes were
included (Table 3). The results for model 5 were similar. The coefficient a ranged between
2.36 and 3.90 and b between 0.41 and 0.51, while the regression between predicted and
observed logDTP resulted in an r2 of 0.89 and s.e. of 0.281, compared to 0.261 for the
calibration where all lakes were included.

3.3. Phosphorus– chlorophyll relationships

Measured mean Chl-a tended to be higher than predicted from the OECD model, but
the difference was not significant and predictions from the other three models did not
differ systematically from measured values (Table 6). Furthermore, calculations based on
observed TP – Chl-a relationships in the reference lakes tended to overestimate Chl-a in the
farm lakes, but again not significantly.

4. Discussion

4.1. Existing models

The traditional phosphorus mass balance models overestimated the effects of farm
emissions on total phosphorus concentration in the included lakes by, on average, a factor of
two. This is an important difference, both from a lake management perspective and for the
fish farming industry. Commercial fish farms require large scale production to be profitable,
and this lower estimate of eutrophication effects could mean that more recipients are
potentially suitable for fish farming. The results are in good agreement with estimates based
on the particulate phosphorus fraction of farm emissions (Beveridge, 1996), but the
estimated farm effects are greater than estimated by Håkanson et al. (1998). It is possible,
but not certain, that the deviations from the old models could be estimated by determining
the size of the rapidly sinking fraction. However, such data was available only for Lake
Skärsjön.
However, although the differences between measurements and predicted values from the
traditional models are significant, there is a large variation between the lakes. This variation
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 205

will, to a certain extent, be caused by the inability of the models to describe the system in
detail, but there is also a considerable uncertainty in empirical data, which will set an ab-
solute limit for how good models can be constructed using this data set. The most important
factors contributing to the uncertainties of the results are the few lakes included in the
regression and the uncertainty in the estimated effects in separate lakes, which in some lakes
are considerable. Besides increasing the confidence intervals of the model predictions, these
factors also increase the risk for stochastic correlations to be misinterpreted as functional
relationships. This is the main reason why we chose to keep the model structures that have
been tested in the older models, instead of introducing new algorithms and driving
variables. The retention time has been shown to affect the retention rates of phosphorus
in the generalized models, and there was also a significant correlation between T and KT in
this work (Fig. 4).
There is also a risk of systematic errors occurring in these results. Some of the lakes
may not have been equilibrated to the new load. There is a weak negative correlation
between the age of the fish farms and departure from the OECD model, i.e. the effects
are closer to the OECD-model predictions in lakes with older fish farms, which may
support such an assumption. Thus, steady-state effects may be higher than the measured
effects. This possibility should be considered when using the models presented in this
work.

4.2. Phosphorus– chlorophyll-a relationships

Since phosphorus and nitrogen are emitted in approximately the same proportions from
all of the studied fish farms, the correlations between farm DTP or DTN and farm-related
increases in Chl-a were similar. The purpose of the Chl-a discussion in this work was
mainly to compare the relationship between nutrient levels and Chl-a in farm lakes with
such relationships in other lakes. Comparisons with phosphorus rather than any other
nutrient was chosen since P was assumed to be the most likely limiting nutrient. In the
Swedish lakes, nitrogen limitation is not likely as the N/P ratios are high and nutrient
concentrations are low or moderately high. In Sweden, nitrogen limitation may occur in
highly polluted lakes, but rarely in the type of lakes included in this study. Nitrogen
limitation may be more likely in Sczcytno Male and Loch Fad, because of their higher
trophic level.
The lakes included in this study are in most cases clear or moderately dystrophic. Light
limitation may occur in the highly eutrophic lakes Sczcytno Male and Loch Fad due to high
phytoplankton concentrations, but probably not in the other lakes.
There was a strong correlation between TP and Chl-a in the fish farm lakes, but it was
not possible to draw any definite conclusions about the differences in farm specific DTP –
DChl-a relationships compared to other phosphorus sources. No significant differences
were found between existing Chl-a models and measurements of Chl-a in farm lakes or
between measured Chl-a– TP relationships in reference lakes and farm lakes (Table 6).
However, the fraction of phosphorus with farm origin in the lakes varied considerably. In
some lakes, the relative farm effects on TP were low, which made it more difficult to detect
differences. Therefore, the conclusions are uncertain, and it would be desirable to test
these relationships on a larger database.
206 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

4.3. Fish farm-specific TP models

The differences in model performance between the tested farm-specific models were
small, and in most cases they will give essentially the same result. The cross validation tests
suggest that the observed relationships are not sensitive to exclusion of single lakes, which
increases the reliability of the results. Still, this should not be confused with a validation
against independent data, which would be a stronger test of model reliability.
It is possible that the strong dominant correlation between DTPin and DTP will distort
the relationships between phosphorus retention (KT or R) and lake sensitivity (T or Dm/T)
in the DTP regressions. It is also difficult to estimate how well the models predict these
underlying relationships. Therefore, the models were also calibrated with DTP/DTPin as
target variable. If the retention rate is independent of the absolute values of TP and TPin,
the best models to use may be the ones calibrated for DTP/DTPin. However, if there are
any relations between KT and DTP or DTPin, they will not be reflected in the calibrations
for DTP/DTPin, but only in the exponents in models 1, 2 and 4 in Table 3. Those exponents
were all close to one, suggesting that the relations between KT and DTP or DTPin are weak
or nonexisting. The small differences in model performance between regressions on DTP
and on DTP/DTPin further support this conclusion. Although all models gave similar
results for the existing database, there are some differences in the predicted relationships
between phosphorus retention and lake sensitivity, expressed as Dm/T or T. The differences
are small for most lakes, but may be important if the models are used for lakes with very
high or low T or Dm/T.
In addition to giving more information on the relationships between phosphorus
retention and sensitivity parameters, the regressions on DTP/DTPin will also be a test of
model reliability, since separate datapoints will affect the regression parameters differently
in the two approaches. Datapoints with high or low values along the x-axis will affect the
slope of the regression line more than values close to the average. For the regression on
DTP/DTPin, the x-value is a function of T or Dm/T, while the loading levels (DTPin) will be
most important for the x-values in the regression on DTP. Similar regression coefficients
would thus indicate a stable relationship. Some differences between the two approaches
should always be expected, since regressions on log(DTP) predict the expected median
value of DTP, while the regressions on logit(DTP/DTPin) predict the median of DTPin/
DTP
1, which is equal to KT*T (Fig. 4). Thus, the former regression will give an
unbiased expected value of the DTP, while the latter will give an unbiased expected value
of the retention rate. This also means that the choice of model depends on the aim of the
investigation. The best result will often be attained using a model calibrated directly for the
target variable. Thus, when the purpose is to predict DTP, models 2– 4 in Table 3 would be
preferred.
Since the differences in model performance were small, it is difficult to conclude which
model is the best. At this stage, the choice of model may instead be based on familiarity
with the model structure and observed sedimentation characteristics of farm emissions. In
Sweden, the OECD model has been used by environmental authorities for a long time, and
it would be most convenient to continue to use this model structure in the future. As to
farm emission characteristics, it is generally accepted that the farm emissions contain a
very fast sinking (cm/s) particulate fraction, which in a mass balance perspective can be
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 207

assumed to be momentarily transported to the sediment (Enell and Löf, 1983; Turrell and
Munro, 1988; Holby and Hall, 1991; Maloney et al., 1992; Ye et al., 1991; Silvert, 1992;
Kelly, 1993; Phillips et al., 1993; Findlay and Watling, 1994; Gowen et al., 1994; Silvert,
1994; Holmer and Kristensen, 1995). Some of this phosphorus will, however, return to the
water column through resuspension and diffusion. Also, there will be some retention of
primarily dissolved or slowly sinking phosphorus fractions. These mechanisms may be
best described by models 2, 4 and 6 in Table 3. They essentially divide the retention of
phosphorus in a momentary removal of a certain fraction of the emissions and retention
according to the generalized models for the rest of the emissions. Of these, model 2 should
be the most appropriate for Swedish conditions, since it is an OECD-type model calibrated
for DTP. When more data become available, there may be reason to reevaluate the model
choice.

4.4. Importance of parameters not included in the model

There are several other parameters that could affect phosphorus dynamics. A number of
drainage area parameters and lake morphometric parameters may be important, but the
correlations between each of these parameters and TP are generally low (Håkanson, 1995).
Of the lake morphometric parameters tested by Håkanson (1995), the depth of the lakes
showed the highest correlation with TP (r =
0.39). It has also been reported that shallow
lakes may be affected for a longer time than deep lakes after external load reductions, due to
a more pronounced internal loading (Forsberg, 1989). There were, however, no clear
relations between lake morphometry and phosphorus elimination in the studied farm lakes in
this work.
Positioning of the fish farm within a lake may also be important. Nutrients emitted far
away from the outlet should remain in the lake for a longer time than if they were emitted
close to the outlet, and should therefore also have a larger effect on nutrient concentrations.
This should be especially important in lakes with low water retention times. The
comparatively large observed effects in Lake Långvattnet seem to support this assumption.
The farm in this lake is located close to the inlet to the lake and the lake is among those where
the effects are closest to Dillon– Rigler/OECD predictions. However, this farm has also been
active for a long time, which could also explain the relatively large effects. The variation
among the other lakes does not seem to correlate with the location of the fish farms, but there
is a tendency for the deviations from the old models to decrease with increasing farm age. It
is therefore possible that some of the lakes were not fully equilibrated to the increased
nutrient loads, which could explain some of the differences between the observed effects and
those predicted with the old models. There are certainly other variables that could also be
important for phosphorus fluxes, e.g. water temperature and other climatic factors, seasonal
patterns for emissions and other lake chemical parameters, but the small database does not
allow a thorough investigation of such parameters.
There were considerable variations in phosphorus concentrations between adjacent years
in many of the lakes, which could not be explained by changes in farm load. These variations
could be caused by changes in land use and other anthropogenic sources, as suggested by
Kelly (1995). However, in most cases it is more likely an effect of the natural variability in
phosphorus fluxes into and within the lakes, driven mainly by climatic factors. We do not try
208 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211

to describe this temporal variation, but such factors could also affect the adequacy of the
reference values. We have therefore chosen lakes where the emissions from the fish farms
dominate the anthropogenic P contributions. Furthermore, the estimated effects are in most
cases based on comparisons with reference locations during the same time periods rather
than, or combined with, time series within the lakes. This should compensate for some of the
natural variation of TP.

4.5. Farm-specific sources of uncertainty

Even though the presented results are promising, there are still considerable uncertainties
in the models (Fig. 5), which has to be considered in practical lake management, e.g. when
evaluating proposed farm permissions. Some of this uncertainty may be related to the use of
old data. The farming techniques and feed composition develop continuously, which affect
the characteristics of the farm emissions. Feed spill has decreased and a larger fraction of
administered phosphorus is utilized by the farmed fish. Thus, the rapidly sinking fraction of
the farm emissions is probably smaller, resulting in decreased gross settling rates. The effect
of these changes on bioavailability of the emitted phosphorus is not clear. It is easy to
assume that the availability of the remaining phosphorus decreases as more of the available
phosphorus is taken up by the farmed fish, but availability tests have shown that the
bioavailability of phosphorus in faeces is usually similar to that in feed pellets (Garzia-Ruiz
and Hall, 1996). It is thus possible that the bioavailability of emitted phosphorus has
remained at approximately the same level despite the changed farming techniques.
Another possible source of error is the assumption that effects of different emissions on
TP are additive. A possible non-additive effect is increased internal phosphorus loading
caused by anoxia in hypolimnion, which would be an effect of increased primary
production, which in turn is caused by increased external nutrient loadings. The assumption
of additivity is, however, well supported by the extensive tests of general phosphorus mass
balance models (e.g. Kirchner and Dillon, 1975; OECD, 1982).

Table 7
Tested range for some important morphometrical, hydrological and chemical variables
Max Min
A (km2) 48 0.16
Dm (m) 15 2.1
Dmax (m) 35 6.2
V (106 m3) 720 0.34
ADA (km2) 733 3.3
Q (106 m3 year
1) 303 1.12
qs (l s
1 km
2) 14 10.8
T (year
1) 4.55 0.01
Production (ton year
1) 255 26
Pfarm (kg year
1) 3757 49
DTPin (mg/m3) 508 1.9
DTP (mg/m3) 100 0.9
TP (mg/m3) 112 6.20
Abbreviations according to Table 1.
 T. Johansson, L. Nordvarg / Aquaculture 212 (2002) 191–211 209

4.6. Practical implications

The models presented in this work are accurate enough to give a first estimate of the
effects of planned fish farms, but the development will naturally need to be monitored in
each case, since there are considerable residual uncertainties in the predictions, and since
there are other important effect parameters that the models do not predict implicitly, e.g.
hypolimnetic oxygen concentrations and phytoplankton biomass. Models are valid only
for the conditions they are tested for. The tested ranges for the models developed in this
project are described in Table 7. Outside these ranges the models will be more uncertain
and should be used with caution.

5. Conclusions

. Existing traditional phosphorus loading models overestimated the effects of fish farm
emissions on TP in most of the included lakes.
. New phosphorus models for fish farm emissions have been presented, based on
Vollenweider and Dillon –Rigler structures. It was not possible to determine which
model type is best suited for this purpose, although Dillon –Rigler models fitted slightly
better to the calibration dataset.
. It was not possible to determine whether the relationship between TP and Chl-a for
farm emitted phosphorus is different from the general relationships found in the
scientific literature.

Acknowledgements

We would like to thank Jan Ekhéll, Germund Mathiasson and Andreas Gyllenhammar
for assistance with the field work. We are also grateful to the fish farmers Hans Bergström,
Ulf Hallin and Leif Olsson, for helping us with sampling and providing farm production
data, and Ann-Charlotte Norborg, Pelle Grahn and Lena af Geijerstam at the county
administration boards of Värmland, Västmanland and Västernorrland, for providing data on
farm production and lake chemistry. This work was funded by contributions from the
European Community Structural Funds: Financial Instrument of Fisheries Guidance
(FIFG).

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