Environ Sci Pollut Res
DOI 10.1007/s11356-015-6015-0
RESEARCH ARTICLE
Modelling the nitrogen loadings from large yellow croaker
(Larimichthys crocea) cage aquaculture
Huiwen Cai 1,3 & Lindsay G. Ross 2 & Trevor C. Telfer 2 & Changwen Wu 1 & Aiyi Zhu 1 &
Sheng Zhao 1 & Meiying Xu 1
Received: 10 August 2015 / Accepted: 22 December 2015
# Springer-Verlag Berlin Heidelberg 2016
Abstract Large yellow croaker (LYC) cage farming is a
rapidly developing industry in the coastal areas of the East
China Sea. However, little is known about the environmental
nutrient loadings resulting from the current aquaculture prac-
tices for this species. In this study, a nitrogenous waste model
was developed for LYC based on thermal growth and bioen-
ergetic theories. The growth model produced a good fit with
the measured data of the growth trajectory of the fish. The total,
dissolved and particulate nitrogen outputs were estimated to be
133, 51 and 82 kg N tonne−1 of fish production, respectively,
with daily dissolved and particulate nitrogen outputs varying
from 69 to 104 and 106 to 181 mg N fish−1, respectively,
during the 2012 operational cycle. Greater than 80 % of the
nitrogen input from feed was predicted to be lost to the envi-
ronment, resulting in low nitrogen retention (<20 %) in the fish
tissues. Ammonia contributed the greatest proportion (>85 %)
of the dissolved nitrogen generated from cage farming. This
nitrogen loading assessment model is the first to address
nitrogenous output from LYC farming and could be a valuable
tool to examine the effects of management and feeding prac-
tices on waste from cage farming. The application of this
Responsible editor: Philippe Garrigues
* Huiwen Cai
caihuiwen1977@hotmail.com
1
National Engineering Research Centre of Marine Facilities
Aquaculture, Zhejiang Ocean University, Zhoushan 316022,
People’s Republic of China
2
Institute of Aquaculture, University of Stirling,
Stirling FK9 4LA, UK
3
No. 1 Haida South Rd, Lincheng, Changzhi Island,
Zhoushan, Zhejiang Province, People’s Republic of China
model could help improve the scientific understanding of off-
shore fish farming systems. Furthermore, the model predicts
that a 63 % reduction in nitrogenous waste production could
be achieved by switching from the use of trash fish for feed to
the use of pelleted feed.
Keywords Dynamic modelling . Large yellow croaker .
Nitrogen loadings . Ammonia . Urea . Cage aquaculture
Introduction
The environmental impact of the waste generated by fish
farming has been the subject of a large number of studies over
the past three decades. It is increasingly becoming a matter of
public concern and government scrutiny worldwide, especially
given the rapid growth of aquaculture as a way to ensure a
secure source of seafood. Particulate or dissolved nitrogen
and phosphorus are significant nutrient waste emissions from
cage farming operations that may lead to environmental degra-
dation, phytoplankton blooms, variations in primary produc-
tion and, consequently, changes in benthic systems when they
enter the surrounding water (Jahan et al. 2003). Reducing the
quantity and impact of these wastes is considered a key element
for the long-term sustainability of the aquaculture industry
(Cho and Bureau 1997). Integrated multi-trophic aquaculture
(IMTA) systems, which are part of the ecosystem approach to
aquaculture (EAA), are designed to improve the environmental
mitigation and sustainability of aquaculture practices (Costa-
Pierce 2013). The application of appropriately balanced diets
also significantly decreases the amount of waste compounds
entering the environment (Hasan 2001).
Most studies quantify the waste loads from aquaculture
operations through field work and tank-based laboratory ex-
periments (Boyd et al. 2001; Ferreira et al. 2008), but mass

balance can also be used to assess the nutrient output
from marine fish farming (Boujard et al. 2002; Cho and
Bureau 1997). Pioneering work on nitrogen and phospho-
rus loadings through mass balance has been conducted for
salmon and rainbow trout farming in Sweden and Northern
Ireland (Ackefors and Enell 1990; Foy and Rosell 1991).
However, although the validity, usefulness and universality
of the nutrient mass balance method has been previously dem-
onstrated in fish and shrimp aquaculture systems (Briggs and
Funge-Smith 1994; Hall et al. 1992; Papatryphon et al. 2005),
estimates of the variation in nutrient output during growth in
relation to the size of the cultured animals has not been well
studied.
The development and application of bioenergetic models
has increased appreciably since the early 1980s. These models
offer valuable information for fish aquaculture and environ-
mental assessment and management, particularly with respect
to evaluating changes in facility size, feeding schedules, feed
composition, water exchange conditions and nutrient loading
(McDonald et al. 1996). Several nutrition-based models have
been proposed to estimate waste outputs from aquaculture
operations (Bureau et al. 2003; Cho and Bureau 1998;
Davies and Slaski 2003; Stigebrandt 1999). Indeed, the appli-
cation of a modified version of the Fish-PrFEQ model has
been adopted as an environmental management tool by the
land-based aquaculture industry in France (Papatryphon et
al. 2005) and proposed for the cage aquaculture industry in
Canada (Azevedo et al. 2011).
Larimichthys crocea (large yellow croaker; LYC) is an im-
portant marine fish species with high commercial value in
countries along the East China Sea, including China, Korea
and Japan. Cage farming of LYC has developed rapidly in
China with production reaching 85,800 tonnes in 2010
(Fishery et al. 2011), and there is the potential for increased
production as offshore cage technology improves. However,
trash fish continue to be used as the traditional feed for
marine carnivorous fish in many Asian countries, and this
practice is likely to persist for some time despite being
regulated or banned in some countries (Gordard 1996).
Farmers are encouraged to use pelleted feed to minimise
farm waste, and some have started using half trash fish and
half pelleted feed. Currently, there is no information on the
impact of the rapid development of the LYC cage farming
industry on feed input, nutrient intake and nitrogen excre-
tion, and there has been no attempt to model the effects of
fish growth on nitrogen output for this important aquaculture
species.
The goal of this study was to develop a bioenergetic-based
nitrogenous waste model for LYC cage farming that incorpo-
rates seasonal temperature variation and different feed types.
Nitrogen retention and the waste output under different feed-
ing practices were also considered in this model, which could
provide a way to estimate the magnitude and seasonal
Environ Sci Pollut Res
variation in nitrogenous waste emissions throughout the
LYC growth cycle. This is the first study to estimate nitrogen
losses from LYC farming and it provides new information on
a non-salmonid species.
Methods and model construction
Study site
The study site is located in the East China Sea near the
Qingbang Islands, China (30° 11.908 N; 122° 41.909 E).
The salinity in this area is 27–33 ‰, water depth varies
between 10 and 40 m and the speed of the water current
is 0.6–0.7 m s−1. Water quality monitoring of this area
began in 2010, and the dissolved oxygen (DO) level is
greater than 6.9 mg L−1, which is well above the mini-
mum requirement for LYC growth (5.0 mg L−1). There is
no stratification in the water column in this area due to
vertical mixing. The fish farm began raising LYC in four
12-m-diameter circular offshore cages with a net depth of
approximately 8 m in 2009; due to the good production
(9.6 tonnage), they expanded to 18 cages (8 cages for
commercial production) in 2012.
As a sub-tropical marine fish species, LYC can survive in
water temperatures ranging from 15 to 25 °C with an optimum
range of 20–22 °C (Ministry of Agriculture and China 2002).
With a stocking density of 5000 fish per cage, the farming
practice commenced in eight cages for commercial pro-
duction on the 5th of July, 2012. The average initial
body weight (IBW) of the fish was 250 g and growing
continued for 150 days before harvest. Trash fish were
used as food for the first 2 months followed by a mix-
ture of trash fish and pelleted feed until the end of the
production cycle. Feed was supplied by hand twice a
day, once before sunrise and once after sunset. Thirty
fish (N = 30) were randomly sampled from the each cage
every 30 days for body weight measurements, and a
group of juvenile LYC with an IBW of 30 g were also
studied for model verification.
Structure of the large yellow croaker waste model
When fish growth rate, environmental temperature and feed
information are known, a bioenergetic model can be used to
estimate food consumption, digestion, excretion and waste
production (Paakkonen et al. 2003; Whitledge et al. 2006).
If the nitrogen in wasted feed is also considered, the total
waste loading of a specific aquaculture operation can be de-
termined. The LYC Waste Model (LYCWM) was developed
in the Vensim® environment (Ventana Systems Inc., Harvard,
MA, USA), and it incorporates three sub-models (fish growth,
food consumption and nitrogenous waste) to simulate fish
Environ Sci Pollut Res

growth and nitrogenous waste emissions under different envi- and t is the time in days. For fish reared at a constant
ronmental conditions during the production period. The struc- temperature, a plot of the cube root of weight against time
ture of the LYCWM system is shown in Fig. 1. yields a straight line. The TGC is calculated in relation to
‘degree-days’ (T × t):

Model components and parameterization p ffiffiffiffiffiffi p ffiffiffiffiffiffiffi 

3
Wt‐ 3 W0
TGC ¼  1000; ð2Þ
Fish growth sub-model T t

Thermal growth coefficient model The most commonly
used fish growth model within the aquaculture industry is
the thermal growth coefficient (TGC) model, in which water
temperature is considered the key controlling factor and food
is not limited (Jobling 2003). The TGC model has been widely
used for management planning due to its ease of use and
flexibility; growth data collected for fish of a given size at
one temperature can be used to predict the growth of fish of
different sizes at other temperatures. The basic formula of the
TGC model is as follows:
p ffiffiffiffiffiffi p ffiffiffiffiffiffiffi
3
Wt ¼ 3 W0 þ ½ðT =1000Þ  t 
where Wt is the final fish weight in grammes, W0 is the
initial fish weight in grammes, T is the temperature in °C
and when a growth prediction is made, the equation be-
comes
npffiffiffiffiffiffiffi o3
Wt ¼ 3
W0 þ ½ðTGC=1000Þ  ðT  t Þ ; ð3Þ
where the growth rate is expressed as (TGC/1000) × (T × t).
As noted by Jobling (2003), using the TGC model to esti-
mate fish growth is only effective if the relationship between
the ratio of the weight and of the length of the fish to the third
power is linear. Based on fish growth data collected from a
number of cages in Huangdun Bay in 2004, fish weight was
ð1Þ
proportional to the body length cubed (Fig. 2), and the TGC
was calculated to be 0.461815. Therefore, the TGC model can
be applied to the LYC growth simulations in this study, and
this TGC value (0.461815) was used in the LYCWM

Stocking density Growth

Fish Produc on
Mortality

Ini al fish mass

Thermal Growth
Growth rate Final fish mass
Coefficient

Food consump on N-wastes N-environment

Ammonia excre on
Temperature rate
Ammonia excreted
Diges bility
Par culate N
Faecal produc on
excreted as faeces
Total Feed input

Diges bility N retained in body

Food conversion
ra o
Total N ingested Total N excreted Urea excreted
Ini al fish mass

Feed N content
Par culate N in
N in Waste feed
waste feed
Waste feed

Fig. 1 Structure of the large yellow croaker waste model. Boxes show functional groupings into sub-models (colour online)

Fig. 2 Length/weight
relationship of large yellow
croaker (colour online)
under the assumption that food and oxygen supplies were
sufficient to meet the requirements of the growing fish.
The relationship between simulated fish body weight and
observed fish growth data was assessed using regression
analysis. All statistical analyses were performed using SPSS
19.0 (SPSS Inc., Chicago, IL, USA).
Temperature
In most bioenergetic-based models, the physiological re-
sponses to environmental conditions are driven by water
temperature, which has a major influence on the metabolic
processes and growth in fish. The diurnal variation in sea
temperature, which is caused by solar radiation and the
earth’s rotation, is very small and usually ignored in nu-
merical modelling (Kawai and Wada 2007), and there is
no temperature stratification due to dynamic vertical
mixing in the study area. Therefore, the use of surface
water temperature is sufficient for modelling purposes.
The surface water temperature in the LYC cage was recorded
daily before feeding using a DO metre (YSI 550A, YSI Inc.,
Yellow Springs, OH, USA).
Food consumption sub-model
Wasted feed was first subtracted from total feed input to
calculate the daily feed ration. When nitrogen content
and digestibility are known, the digestible fractions of
proteins, lipids and carbohydrates can be calculated, and
the feed conversion ratio can be used to determine the
incorporation of nitrogen into the body and its faecal
excretion. When the nitrogen in wasted feed is also
considered, the waste loading of a specific aquaculture
Environ Sci Pollut Res
operation can be quantified. A typical input–output algorithm
can be expressed as follows:
Feed input N ¼ Feed wastage N þ Faecal N þ Excreted N ð4Þ
þ N Retained in body
Feeding
The feeding parameters used in the model were based on the
actual feeding regime in the LYC cages at the farm. A com-
bined feeding strategy was employed; LYC were fed trash fish
during the first 2 months of growth with a daily feeding ration
of 5 % of fish body weight. After the 2 months, fish were fed a
50:50 mixture of trash fish and 4.5-mm pelleted feed over the
next 3 months with a feeding ration of 1.5 % of fish body
weight (Table 1). The trash fish were caught by trawlers and
fixed nets and were primarily a mixture of Pneumatophorus
japonicus, Collichthys lucidus and Coilia spp., which have
low commercial value but high production rates in the East
China Sea during the summer. The pelleted feed was supplied
by the Ningbo fish feed company.
Wastage rate
It is difficult to separate wasted feed from other solid wastes
due to variations in the properties of particulate wastes.
Nevertheless, food wastage values have been reported to
range between 1 and 40 % (Beveridge et al. 1991), and trash
fish feed always has a higher wastage rate than pelleted feed
due to its low utilisation. A trash fish wastage rate of 30–46 %
was reported by Leung et al. (1999b) for grouper (Epinephelus
areolatus), and wastage rates of 52 and 30 % were found for
trash fish and pelleted feed, respectively, based on survey data
Environ Sci Pollut Res

Table 1 Nutrient content of

different feeds for large yellow Feed Water Protein Lipid Carbohydrate Ash
croaker (% wet weight)
Trash fisha Pneumatophorus japonicas 69.10 19.90 7.40 2.20 1.40
Collichthys lucidus 74.80 18.90 5.00 / 1.30
Coilia spp. 73.30 17.70 4.90 3.10 1.00
Trash fish mean 72.40 18.75 5.77 1.77 1.23
Pelleted feedb 5.76 46.41 9.58 36.79 1.46
a
Food Technology China (http://www.tech-food.com)
b
Ningbo Tech-Bank Company Limited

from LYC cage farms. Based on these data, feed wast-
age rates of 52 and 41 % (the mean values of trash fish
and pelleted feed) were used for trash fish feeding and
mixed feeding, respectively.
Digestibility
Although trash fish has a high wastage rate, the enzymes in
trash fish can result in digestibility as high as 98 % when
consumed (Jobling 1994). Trials using different types of
manufactured pelleted feed for LYC have reported relatively
low protein digestibility of between 75 and 88 % (Cai et al.
2006). Based on the feeding regime used in this study, the
digestibility of trash fish was estimated to be 93 %, and the
digestibility of the mixed feed was estimated to be 91 % (the
mean values of the two types of feed).
Nitrogenous waste sub-model
In marine teleosts, the dissolved nitrogen excreted via the gills
is composed of ammonia, urea and other soluble compounds,
with ammonia being the largest fraction. Ammonia excretion
rates in fish are influenced by temperature and fish size, so a
temperature- and body weight-dependent rate was used in our
model (Eq. 5), which was developed by Wang and Yan (2008)
based on LYC ammonia excretion field data (Sun et al., 2004).
Ammonia excretion was calculated as follows:
TAN ¼ 12:612  W ‐0:033  T 0:935 ;
where TAN is the total ammonia-N excretion rate
(mg N kg fish−1 day−1), T is the temperature (°C), and W is
the fish body weight (kg).
Although there are different estimates of urea excretion
rates, LYC urea production data were not available.
Therefore, urea production was assumed to be the differ-
ence between the total dissolved nitrogen excretion and
the total ammonia excretion throughout the entire growth
period (Eq. 6).
Urea excreted ¼ Dissolved nitrogen – Ammonia excreted ð6Þ
Investigation of the effects of different feeding strategies
on nitrogen excretion
The type of feed impacts digestibility and the subsequent ni-
trogen excretion due to the differences in protein, lipid, water
and other nutritional contents between different feed types. By
changing key parameters (e.g. feed type, protein content, di-
gestibility), it was possible to use the model to investigate
nitrogenous waste production under different potential feed-
ing regimes. Three scenarios were used in the model: (a) trash
fish only, (b) a 50:50 mixture of trash fish and pelleted feed
and (c) pelleted feed only.
Results
The complete model was developed to simulate fish growth
and nitrogenous waste production and account for the major
factors influencing growth including water temperature and
feed type. The model was based on environmental and LYC
growth data from the 2012 growing season and was verified
with directly measured growth data from juvenile LYC farmed
at the same site.
Fish growth
Initial body weight, TGC and daily temperature data were
used as inputs for the fish growth sub-model to predict growth
from July to December. The daily increase in body mass (daily
ð5Þ growth rate) and the final fish body mass at the end of each
day are presented in Figs. 3 and 4c. The results show that fish
body weight steadily increased with time but at different daily
growth rates. Water temperature was included in the model to
determine its effects on fish growth, metabolic rate and nitro-
gen emission. During the 2012 production cycle, the temper-
ature of the sea water in which the fish were raised ranged
from 16 to 27 °C, which is suitable for LYC cultivation
(Fig. 4a). The fastest and the slowest changes in daily body
weight were observed in August (1.97 g day−1) and December
(1.46 g day−1), indicating an influence of temperature on
growth (Fig. 4a).

Fig. 3 Modelled daily body mass
increment of LYC during the
2012 production cycle
There was a high correlation between the modelled and
measured fish body weights (r = 0.98, p = 0.001) (Table 2).
For the first 4 months, the predicted fish body weight was
slightly lower than the actual value, but it was slightly higher
in the last month. The maximum discrepancy between the
simulated results and the field data was less than 9 %,
suggesting that the model provided realistic estimates of
LYC growth. The growth of the juvenile LYC (IBW = 30.7 g)
was also simulated and validated by the measured data,
and the discrepancy was less than 13 % between the
actual and modelled results (Table 3). The results demonstrate
that the LYCWM is suitable for estimating the growth
of 30–550 g LYC.
Fig. 4 The relationship between
temperature (a), ammonia
excretion rate (b) and fish body
mass (c)
Environ Sci Pollut Res
Nitrogen mass balance
The nitrogenous outputs from the aquaculture system were
simulated using the feed consumption and nitrogenous waste
production sub-models and the nitrogen mass balance equa-
tion (Eq. 4). The results of the simulation (Table 4) showed
that the major nitrogenous waste component was particulate
nitrogen, which accounted for more than 46 % of the faecal
matter excreted by the fish and wasted food. The particulate
nitrogen fraction was reduced following the change to pelleted
feed after day 60, and dissolved nitrogen, which consisted of
ammonia, urea and other nitrogenous compounds excreted
through the gills, kidneys and skin, accounted for 27 % of
Environ Sci Pollut Res

Table 2 Comparison of
modelled and measured fish Time (days) Month Temperature (°C) Modelled Measured Discrepancy
weights of large yellow croaker in results (g) weight (g) (g (%))
the 2012 production cycle (fish
number = 30) 1 Jul. 26.0 275.00 275.00 0.00 (0)
30 Aug. 25.5 322.26 345.00 −22.74 (−6.59)
60 Sep. 26.0 375.67 410.00 −34.33 (−8.37)
90 Oct. 23.0 432.42 475.00 −42.58 (−8.96)
120 Nov. 21.0 487.60 520.00 −32.40 (−6.23)
150 Dec. 16.0 536.67 525.00 11.67 (2.22)

the feed nitrogen input and increased to 34 % after the change
in diet. The retention of nitrogen in the body increased from
17.6 to 19.5 % after the change in feed, and the nitrogen
content of the LYC was estimated to be 16.43 g (nitrogen
content was assumed to be constant at 3.06 %) with a final
fish weight of 537 g at the end of the culture operation. The
predicted nitrogen accumulation in the fish for the entire
growth period was 8 g, and adding this value to the initial
nitrogen content of 8.42 g yielded a final estimated nitrogen
content of 16.42 g. This agreed closely with the actual nitro-
gen content of the fish at harvest.
Nitrogenous waste production
The LYCWM provided a way to estimate the magnitude of the
daily nitrogenous waste output by considering variations in
water temperature and changes to the feeding strategy. Four
different nitrogenous waste estimates from LYC cage farming
were predicted by the model: particulate nitrogen from wasted
feed and faecal matter, total dissolved nitrogen and individual
estimates of dissolved ammonia and urea. Total nitrogen,
which was the sum of the dissolved and particulate nitrogen,
was also considered. Under current farming practices, the en-
vironmental nitrogen load from producing 1000 kg of LYC
has been estimated to be 133 kg of total nitrogen, of which
82 kg is particulate and 51 kg is dissolved, and the latter
consists of 45 kg of ammonia and 5.9 kg of urea. Of the total
feed nitrogen input, approximately 80 % was released into the
environment, which is equivalent to an annual discharge of
approximately 1143, 438, 705, 387 and 51 kg of total
nitrogen, dissolved nitrogen, particulate nitrogen, ammonia
and urea, respectively, based on the total LYC production of
19.6 tonnes at the study site in 2012.
Particulate nitrogen
The daily particulate nitrogen emission over the 2012 rearing
season is presented in Fig. 5. A peak in particulate nitrogen
output of 181 mg N day−1 fish−1 occurred early in the cultur-
ing period when the water temperature was 25–27 °C, which
resulted in high food consumption and growth rates. A
marked decrease occurred over several days due to the change
in feed after day 60. During this period, the fish were probably
acclimating to the new feed, which affected consumption,
digestion, metabolism, excretion and waste production.
Particulate nitrogen output decreased to 106 mg N d−1 fish−1
near the end of the culture cycle after a period of stable nitro-
gen output.
Dissolved nitrogen
It can be assumed that ingested nitrogen, which was not
retained for growth or released as faeces, was metabolised
and then excreted as dissolved nitrogenous products, primar-
ily ammonia and urea. The modelled dissolved nitrogen ex-
cretion varied from 69 to 104 mg N day−1 fish−1 with water
temperature and fish body weight (Fig. 5), and peak dissolved
nitrogen emission (95 to 104 mg N day−1 fish−1) occurred over
a 55-day period of high and stable fish growth from days 65 to
120 (mid-September to November). During the final month of

Table 3 Comparison of
modelled and measured fish Time (days) Month Temperature Modelled weight (g) Measured weight (g) Discrepancy (g (%))
weight of juvenile large yellow (°C)
croaker in the 2012 production
cycle (fish number = 30) 1 Jul. 26.0 30.70 30.70 0.00 (0)
30 Aug. 25.5 41.86 40.80 1.06 (2.60)
60 Sep. 26.0 56.27 54.70 1.57 (2.87)
90 Oct. 23.0 73.00 67.50 5.50 (8.15)
120 Nov. 21.0 90.46 80.30 10.06 (12.65)
 Environ Sci Pollut Res

Table 4 Modelled monthly

nitrogen budget of large yellow Time (days) 1 30 60 90 120 150
croaker in the 2012 production
cycle N in feed (mg) 265.00 288.00 326.00 285.00 282.00 229.00
Body retained N (mg) 46.70 50.73 57.29 55.68 55.09 44.76
Particulate N (mg) 147.00 159.69 180.36 131.97 130.56 106.08
Dissolved N (mg) 71.84 78.04 88.14 97.32 96.27 78.23
N in feed (%) 100.00 100.00 100.00 100.00 100.00 100.00
Body retained N (%) 17.62 17.61 17.57 19.54 19.54 19.55
Particulate N (%) 55.47 55.45 55.33 46.31 46.30 46.32
Dissolved N (%) 27.11 27.10 27.04 34.15 34.14 34.16

culture, fish biomass was greatest, which should have resulted
in high production of dissolved nitrogen. However, the drop in
water temperature and the associated decrease in food con-
sumption and excretion resulted in low dissolved nitrogenous
waste production.
According to the results of the field monitoring in 2012,
there was a significant increase in the concentration of dissolved
inorganic nitrogen from July to December (July = 0.20 mg L−1;
September = 0.81 mg L−1; November = 0.55 mg L−1). The pre-
dicted trend in dissolved nitrogen output agreed with the ob-
served variation in dissolved nitrogen concentration, suggesting
that the model produced realistic estimates of nitrogen output.
Ammonia
In our simulated results, ammonia was the main form of dis-
solved nitrogen produced during LYC farming and it
accounted for approximately 84–94 % of the total dissolved
nitrogen produced (Table 5). The estimated ammonia excretion
rate by LYC ranged from 137 to 230.5 mg N kg fish−1 day−1,
which was very similar to that found in laboratory experiments
(96.8–279.7 mg N kg fish−1 day−1) in Huangdun Bay, China.
The daily estimated ammonia emission by the specific fish in
our model varied from 59 to 89 mg N day−1 fish−1 indicating a
correlation with the changes in water temperature and fish
biomass (Fig. 6). There was an ammonia emission peak in
August, and a decreasing trend was observed towards the
end of the cycle as the temperature dropped.
Urea
Urea excretion was much lower than ammonia excretion over
the entire growth cycle with values ranging from 4.8 to
17.5 mg N day−1 fish−1 (Fig. 7), which accounted for 6–
15 % of the total dissolved nitrogen generated (Table 5).
Although the pattern was less clear, this variation did appear
to correlate with the variation in water temperature and fish
growth rates. The marked change in urea production at day 60
reflects the change in feed from trash fish to a mixed diet.
Impact of feeding strategy on modelled nitrogen
production
Feed quantity and quality directly affects the growth and met-
abolic processes of fish as well as the production of nitroge-
nous waste. Nitrogen emissions under three feeding scenarios,

Fig. 5 Modelled daily particulate

and dissolved nitrogen emission
of LYC during the 2012
production cycle (colour online)
Environ Sci Pollut Res

Table 5 Modelled daily

ammonia and urea emission of Time (days) 1 30 60 90 120 150
large yellow croaker
Dissolved N (mg day−1 fish−1) 71.84 78.04 88.14 97.32 96.27 78.23
Ammonia (mg day−1 fish−1) 60.95 69.40 81.96 83.74 86.38 73.49
Urea (mg day−1 fish−1) 10.89 8.64 6.18 13.58 9.89 4.73
Ammonia (%) 84.83 88.92 92.99 86.05 89.72 93.95
Urea (%) 15.17 11.08 7.01 13.95 10.28 6.05

(1) traditional (trash fish), (2) current (mixed feed) and (3)
future (pelleted feed), are presented in Fig. 8. The following
daily dissolved nitrogen production values were obtained over
the 150 days of the culturing cycle: 56–75 mg N day−1 fish−1
for pelleted feed; 69–93 mg N day−1 fish−1 for trash fish and
78–105 mg N day−1 fish−1 for mixed feed) (Fig. 8a). The daily
particulate nitrogen output was highest in scenario 1, which
was 2.5 times higher than with pelleted feed (Fig. 8b).
However, faecal nitrogen was lowest under the trash fish feed-
ing regime (Fig. 8c) because trash fish are usually highly di-
gestible due to their high enzymatic activity and water content.
By contrast, feeding trash fish to LYC clearly resulted in the
highest amount of nitrogenous waste from uneaten feed (132–
178 mg N day−1 fish−1), whereas pelleted feed produced the
least (49–66 mg N day−1 fish−1) and reduced nitrogen emis-
sions relative to trash fish feed by 63 % (Fig. 8d).
To produce 1000 kg of LYC, the total nitrogen, dissolved
nitrogen and particulate nitrogen emissions under the three
scenarios were as follows: 143, 47 and 96 kg, respectively,
for scenario 1; 133, 51 and 82 kg, respectively, for scenario 2
and 81, 38 and 43 kg, respectively, for scenario 3. The nitrog-
enous waste production was closely related to the quality,
nutrient composition and digestibility of the feed, and the four
forms of nitrogen production in the model were estimated to
increase with increasing protein content in the feed (Table 6),
especially the production of dissolved nitrogen. The estimated
production of dissolved nitrogen almost doubled when the
protein content increased from 40 to 60 %. In addition, im-
proving the digestibility of the feed resulted in higher dis-
solved nitrogen emissions, even though particulate nitrogen
output significantly decreased, especially the nitrogen in fae-
cal matter (Table 6).
Discussion
In this study, a fish growth and nitrogenous waste production
model (LYCWM) was developed based on a bioenergetic
framework and used to predict nutrient loading from offshore
LYC cage farming. Bioenergetic and nutritional models have
been successfully used for loading assessments of fish farms
and hatcheries (Cho and Bureau 1998; Azevedo et al. 2011).
In the present study, the model was calibrated with measured
fish growth data, which showed a less than 13 % discrepancy
with the bioenergetic model. Past studies using other fish
growth models have shown large deviations from the
observed data, ranging from −86 to +770 % depending
on the species (Ney 1993). Only a few bioenergetic model
studies have shown reasonable consistency with measured
data (discrepancies of less than 15 %) (e.g. 0.3–3.2 % for lake

Fig. 6 Modelled daily ammonia

excretion of LYC during the 2012
production cycle
 Environ Sci Pollut Res

Fig. 7 Modelled daily urea

emission of LYC during the 2012
production cycle

trout (Salvelinus namaycush) (Madenjian and O'Connor Our model provided a satisfactory estimation of LYC
1999), 8 % for largemouth bass (Micropterus salmoides) growth before sexual maturity (body weight of 30–550 g),
(Rice and Cochran 1984), and 10 % for sockeye salmon which is representative of the size of fish used in commercial
(Oncorhynchus nerka) (Beauchamp et al. 1989)). farming practices. To reduce the risk of mortality in offshore

Fig. 8 Effects of different feeding scenarios on nitrogen emissions from LYC. a Dissolved nitrogen. b Particulate nitrogen. c Faecal nitrogen. d Nitrogen
in waste feed
Environ Sci Pollut Res

Table 6 Impact of feed variation on nitrogen production

Parameters varied FCR Wastage Digestibility Feed N Dissolved Particulate Feed nitrogen Faecal
rate (%) (%) content (%) nitrogen nitrogen wastes nitrogen
(mg N day−1) (mg N day−1) (mg N day−1) (mg N day−1)

Feed scenarios Trash fish 5.8 52 93 3 68.7–92.6 140.6–189.4 132.1–177.9 8.5–11.5

Mixed feed 3 41 91 5.22 78.1–105.2 105.9–142.6 93.7–126.2 12.1–16.4
Pelleted feed 1.5 30 88 7.43 55.6–74.8 62.5–85.1 48.8–65.7 13.7–18.4
N content (assuming protein 60 % 1.5 30 88 9.6 84.8–114.2 80.7–108.7 63.1–84.9 17.7–23.8
pelleted feed) protein 50 % 1.5 30 88 8 63.3–85.2 67.3–90.6 52.6–70.8 14.7–19.8
protein 40 % 1.5 30 88 6.4 41.7–56.1 53.8–72.5 42.1–56.6 11.8–15.9
Digestibility (assuming 90 % 1.5 30 90 7.43 57.8–77.9 60.2–81.1 48.8–65.7 11.4–15.3
pelleted feed) 88 % 1.5 30 88 7.43 55.6–74.8 62.5–85.1 48.8–65.7 13.7–18.4
83 % 1.5 30 83 7.43 49.9–67.2 68.2–91.8 48.8–65.7 19.4–26

cage farming, farmers prefer to stock fish that are 30–100 g
and harvest them at approximately 500–600 g, which is before
sexual maturity when the growth rate declines. The existence
of growth stanzas from various fish species emphasises the
need to use different growth functions in model design to
better fit the specific growth patterns. Dumas et al. (2007)
defined three growth stanzas in the rainbow trout life cycle
(<20, 20–500 and >500 g) with different estimated weight
exponents. Chowdhury et al. (2013) determined the growth
trajectory of tilapia using different growth models for the nurs-
ery stage (1–30 g), the pre-grow-out stage (30–220 g) and the
grow-out stage (>220 g).
Temperature is the key environmental factor affecting in-
gestion, metabolism and growth in fish, and our model pro-
vided a way of estimating the seasonal variation in fish growth
and waste output throughout the culturing cycle by accounting
for daily variations in temperature. The daily biomass incre-
ment decreased in later November and December when the
temperature was low. LYC metabolism slows when the tem-
perature drops to 18 °C, and at less than 15 °C, the feeding
regime is changed to once every 2 days to accommodate this
reduced metabolism (Ministry of Agriculture and China
2002). In this case, it is difficult to simulate metabolic rate,
which may explain why the fish growth sub-model slightly
overestimated the increase in biomass in the final month.
Temperature-related changes in feed intake and metabolism
resulted in a significant change in waste output over
time, which is important for assessing the environmental
impact and determining management strategies. The
peak period of dissolved nitrogen emission occurred
from mid-September to early November in this study,
which was consistent with a study by Davies and
Slaski (2003) in which higher waste output occurred from
August to September in Atlantic halibut (Hippoglossus
hippoglossus, L.). It is important to know total waste loading
from cage farming in a specific area; however, other impor-
tant factors that could impact the environment (e.g. seasonal
variations compared to daily or weekly waste emissions) are
also necessarily to be considered properly.
The total nitrogenous waste production in the 2012 culture
cycle was 133 kg N tonne−1 of fish production, and similar
values have been reported for other carnivorous fish fed with
trash fish, such as grouper (170.6 kg N tonne−1 of fish pro-
duction) (Leung et al. 1999a), whereas a higher output of 224–
462 kg N tonne−1 was reported for bluefin tuna (Thunnus
maccoyii) (Fernandes et al. 2007). Particulate nitrogen
accounted for 58–67 % of nitrogenous wastes and varied de-
pending on the type of feed used. A significant decrease of
37.6 % was found for daily particulate nitrogen production
when changing from the mixed feed, which is currently used,
to pelleted feed. This suggests that environmental impacts
from aquaculture can be reduced with the use of pelleted
feed, and Chu (2002) reported higher nitrogen loading (a 17-
fold increase) from grouper in Hong Kong when fed trash fish
instead of moist pellets (20 % lipid, 50 % protein). The devel-
opment of high-quality pelleted feed specific to different spe-
cies as a replacement for trash fish is one of the most important
and urgent concerns of the sustainable fish farming industry in
China and other Asian countries.
Based on the limited research on marine teleost species,
urea production appears to remain fairly constant and
comprises approximately 20 % of dissolved nitrogenous
waste (Wright and Anderson 2001). In the present study,
6–15 % of dissolved nitrogenous waste from the cage
farming was estimated to be excreted as urea, which
ranged from 0.37 to 1.85 mg kg−1 h−1 for LYC cultured
in 2012. Similar data have been reported for sea bass
(0.66–1.16 mg kg−1 h−1) (Guerin-Ancey 1976) and for
blenny and dab (0.53 and 0.51 mg kg−1 h−1, respectively)
(Sayer and Davenport 1987). Additionally, a very high
rate of urea excretion (60–80 mg kg−1 h−1) after feeding
was found for cape anchovy (James et al. 1989). The
large variation in urea production among species indicates
that urea excretion may be species-specific.

Ammonia is the major component of the dissolved nitrogen
output (85 % of total nitrogen output), and it generally in-
creases with increases in feed intake, protein synthesis and
overall metabolic rate, which occurs as temperatures rise
(Wright and Anderson 2001). The positive relationship be-
tween temperature and the ammonia excretion rate was sig-
nificant (Fig. 4), which is consistent with the data of Leung et
al. (1999a). In our study, a high ammonia emission rate
(86 mg N day−1 fish−1) was found when the temperature
was above 22 °C. Jobling (1994) found that ammonia excre-
tion in rainbow trout at 20 °C (77 mg N day−1) was 2.75 times
higher than that at 10 °C (28 mg N day−1).
As observed in LYC (Fig. 4), Porter et al. (1987) noted
a significant size-related decrease in the TAN excretion
rate in sea bream after feeding at 24.2 °C (70, 36.4 and
25.2 mg N kg−1 body wt h−1 for fish weighing 3, 40 and
90 g, respectively). However, due to the very limited am-
monia excretion data available for LYC, the effect of die-
tary protein level was not included in the present study. A
similar species, the areolated grouper (E. areolatus), was
found to have an average ammonia excretion rate of
375.7 mg N kg−1 body wt day−1 after feeding on trash
fish at 25 °C (Leung et al. 1999a). A TAN excretion rate
of 133.7 mg N kg−1 body wt day−1 has been reported for
red grouper fed with minced fish at 21–22 °C (Ove Arup
et al. 1989). A maximum ammonia excretion rate of
600 mg N kg−1 h−1 has been reported for cape anchovy
after feeding (James et al. 1989), which emphasises the
effects of feeding on ammonia excretion.
Nitrogenous waste emission is directly related to digestibil-
ity, which can be affected by feeding or starving the fish, as
well as feed composition. In carnivorous fish, the absorption
efficiency usually ranges from 70 to 95 % when consuming
natural prey (Jobling 1994), but the characteristics of for-
mulated feeds are radically different from natural prey or-
ganisms in terms of moisture, energy content and nutrition-
al composition. Natural prey has a relatively high water
content (55–89 %) with an energy content of 3–12 kJ g−1
wet weight (Zhang et al. 2008), whereas the moisture con-
tent of commercial feeds is usually 10 % or less with an
energy content of 20–25 kJ g−1. A high protein digestibility
value (95 %) was found for both LYC and sea bass when
fed with trash fish, but the digestibility of pelleted feed was
lower (88 %) (Cai et al. 2006). The high water content
makes natural prey easier to digest, and the active enzymes
in trash fish, which are not present in pelleted feed, aid the
digestion process (Guan et al. 2007). By contrast, low di-
gestibility of trash fish was reported by Carter et al. (1999)
in bluefin tuna (73 %) resulting in high faecal excretion.
An increase in faecal nitrogen production of 42 % was
found in this study when the digestibility was reduced from
88 to 83 %. A fivefold increase in the faecal excretion rate
has been reported in both Atlantic cod (Gadus morhua) and
Environ Sci Pollut Res
turbot (Scophthalmus maximus) when the nitrogen assimi-
lation efficiency was reduced from 99 to 95 % (Bromley
1987; Santos and Jobling 1991).
The fraction of nitrogen retained for fish growth can vary
from 7 to 40 % of the feed nitrogen input depending on the
cultured species and the operations of the farm (Fernandes et
al. 2007). Low nitrogen retention (less than 20 %) was found
in the present study, and sea bass have been reported to have a
nitrogen retention of 15–20 % (Roque D’Orbcastel and
Blancheton 2006). Lower body retention values in fish often
result from the use of trash fish as feed (e.g. <12 % for bluefin
tuna (Fernandes et al. 2007), <12 % for grouper (Leung et al.
1999b) and <18 % for LYC (present study)). Values for some
well-studied aquaculture species are often much higher
when high quality pelleted feed is used (e.g. up to 40 %
for Atlantic salmon (Strain and Hargrave 2005) and 27–
28 % for rainbow trout (Hall et al. 1992)). This indicates
that digestibility and feed utilisation are both important for
nitrogen retention in fish.
Conclusion
In summary, the LYCWM proposed in this study was con-
structed based on an understanding of fish bioenergetics, and
it considered variations in key variables, such as temperature
and feed type. The application of our model provided reliable
fish growth and waste output information; however, as with
most models, it is important to recognise that there is still some
level of uncertainty. Further work to improve the data param-
eters and assumptions of the model is required to generate
more accurate predictions. Nevertheless, this model provides
a good estimate of fish growth and of particulate and dissolved
nitrogen emissions for fish of a given size for different feeding
regimes. Improvements in feed quality and changes in feeding
strategy, such as changing from trash fish to pelleted feed,
could significantly decrease the amount of waste released to
the environment. This could lead to improved carrying capac-
ities and, ultimately, sustainable aquaculture practices.
Acknowledgments This work was funded by National Natural Science
Foundation of China (41206088), Ministry of Science and Technology of
People’s Republic of China (2012BAB16B02, 2011BAD13B08), State
Oceanic Administration (201305009–2, 201305009–3), Natural Science
Foundation of Zhejiang Province (LQ12D06001), Bureau of Science and
Technology of Zhoushan (2015C41002), PECRE award from Marine
Alliance for Science and Technology for Scotland (MASTS) and Youth
Teachers’ Program of Zhejiang Ocean University. Some data used are
unpublished from EU 6FP INCO SPEAR project (2004–2007). We thank
Dr. Kim Jauncey for his constructive comments during this study.
Compliance with Ethical Standards
Conflict of interest The authors declare that they have no competing
interests.
Environ Sci Pollut Res
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