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There have been some arguments concerning supplementary feed (cereals) based common carp production in fishponds and water pollution, mostly in Central Europe. Using Czech Republic (top producer in EU) as a benchmark and combining data on nutrient digestibility of feedstuffs used combined with analyses of literature data, we have assessed – nutrient footprint (∼9.4–10.8 kg N ha−1, ∼2.7–3.2 kg P ha−1; 1.5–4 × < EU crop-livestock sectors); nutrient utilization efficiencies (NUEN ∼36%, NUEP ∼50%; 1.5–1.7 × > EU livestock average); autochthonous nutrient removal (∼8–9.2 kg N ha−1, 1.4–1.6 kg P ha−1); eco-cost burden (13–29 × ≪ positive services); eco-services (∼74.5–100.6 million € country−1; ∼2375 € ha−1) of carp production in Central Eastern European Region (CEER). Digestible nutrients offered by natural prey (7.9% N, 1% P on dry matter basis) to carp are ∼5–8 times higher than those provided by cereals and remains the key determinant for production. Despite this, 70–90% of nutrient footprint from feeding is contributed by cereals. Neutral footprint (∼374 kg ha−1) and exclusively natural (up to 300 kg ha−1) carp production intensities were identified, following which, commercial interest of carp farming may falter (costing intangible losses >56.5 million € in CEER), despite achieving ‘greener-goals’. Per production cycle, carp aquaculture in CEER fishponds offer at least 579 million € worth of services. Our results show that carp production in ponds have lesser nutrient burden than crop and livestock productions in EU. Existing management of fishponds ‘barely meet’ optimum P requirements of common carp and present production intensity should not be vilified as a pollution causing activity. Risks and solutions for achieving both environmental (minimized footprint) and aquaculture goals (uncompromised production) are discussed.
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Nutrient footprint and ecosystem services of carp production in
European shponds in contrast to EU crop and livestock sectors
Koushik Roy
a
, Jaroslav Vrba
b
, Sadasivam J. Kaushik
c
, Jan Mraz
a
,
*
a
University of South Bohemia in Ceske Budejovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and
Biodiversity of Hydrocenoses, Institute of Aquaculture and Protection of Waters,
Cesk
e Bud
ejovice, 370 05, Czech Republic
b
University of South Bohemia in Ceske Budejovice, Faculty of Science, Department of Ecosystem Biology,
Cesk
e Bud
ejovice, 370 05, Czech Republic
c
European Research Area (ERA) Chair, EcoAqua, Universidad de Las Palmas de Gran Canaria, Taliarte, 35214, Telde, Las Palmas, Canary Islands, Spain
article info
Article history:
Received 5 November 2019
Received in revised form
20 March 2020
Accepted 14 May 2020
Available online 8 June 2020
Handling editor: Prof. Jiri Jaromir Kleme
s
Keywords:
Nitrogen and phosphorus
Nutrient utilization efciency
Eutrophication
Environmental burden and ecosystem
services
EU agriculture And livestock sectors
Cleaner production
abstract
There have been some arguments concerning supplementary feed (cereals) based common carp pro-
duction in shponds and water pollution, mostly in Central Europe. Using Czech Republic (top producer
in EU) as a benchmark and combining data on nutrient digestibility of feedstuffs used combined with
analyses of literature data, we have assessed enutrient footprint (~9.4e10.8 kg N ha
1
, ~2.7e3.2 kg P
ha
1
;1.5e4<EU crop-livestock sectors); nutrient utilization efciencies (NUE
N
~36%, NUE
P
~50%; 1.5
e1.7 >EU livestock average); autochthonous nutrient removal (~8e9.2 kg N ha
1
,1.4e1.6 k g P ha
1
);
eco-cost burden (13e29 positive services); eco-services (~74.5e100.6 million Vcountry
1
; ~2375 V
ha
1
) of carp production in Central Eastern European Region (CEER). Digestible nutrients offered by
natural prey (7.9% N, 1% P on dry matter basis) to carp are ~5e8 times higher than those provided by
cereals and remains the key determinant for production. Despite this, 70e90% of nutrient footprint from
feeding is contributed by cereals. Neutral footprint (~374 kg ha
1
) and exclusively natural (up to
300 kg ha
1
) carp production intensities were identied, following which, commercial interest of carp
farming may falter (costing intangible losses >56.5 million Vin CEER), despite achieving greener-goals.
Per production cycle, carp aquaculture in CEER shponds offer at least 579 million Vworth of services.
Our results show that carp production in ponds have lesser nutrient burden than crop and livestock
productions in EU. Existing management of shponds barely meetoptimum P requirements of common
carp and present production intensity should not be vilied as a pollution causing activity. Risks and
solutions for achieving both environmental (minimized footprint) and aquaculture goals (uncompro-
mised production) are discussed.
©2020 Elsevier Ltd. All rights reserved.
1. Introduction
For decades, the land-lockedcentral European countries have
been relying mostly on carp culture for sheries production
(Ad
amek et al., 2012;G
al et al., 2015;Woynarovich et al., 2011).
Common carp (Cyprinus carpio L.) farming in shponds has
remained the mainstay, both traditionally and commercially (G
al
et al., 2015). About 80e88% of the aquaculture production in
these countries come from carp farming in shponds (Eurostat
sh_aq2a 2017). Czech Republic followed by Poland, Hungary and
Germany (ranked in order of production) support ~80% of carp
production in the European Union (EU) (Eurostat sh_aq2a 2017).
The apparent per capita consumption of carp in the region varies
between 0.6 and 1.2 kg (EUMOFA, 2016). Since the late 1960s, carp
farming in Europe has undergone intensication with yield
<190 k g ha
1
to >450 kg ha
1
(Pechar, 2000). The higher stocking
density corresponded higher input of supplementary feed. Today,
about 86% of Czech shponds involved in production are fed with
supplementary feed, mostly cereals (CZ-Ryby, 2019). Present
practices include semi-intensive farming with a low to moderate
stocking density (0.2e0.4 ton ha
1
) and having a production ceiling
of ~0.5e1 ton ha
1
, partly supported by supplementary feeding
(Sterni
sa et al., 2017). In most of these shponds, ~50e60% of carp
growth (protein growth) is believed to be supported by natural food
while cereals (rich source of energy) are provided as
*Corresponding author. Institute of Aquaculture and Protection of Waters, Fac-
ulty of Fisheries and Protection of Waters, University of South Bohemia in Ceske
Budejovice, Na Sadkach, 1780, Ceske Budejovice, 370 05, Czech Republic.
E-mail address: jmraz@frov.jcu.cz (J. Mraz).
Contents lists available at ScienceDirect
Journal of Cleaner Production
journal homepage: www.elsevier.com/locate/jclepro
https://doi.org/10.1016/j.jclepro.2020.122268
0959-6526/©2020 Elsevier Ltd. All rights reserved.
Journal of Cleaner Production 270 (2020) 122268
supplementary feed (Ad
amek et al., 2009,2012). This co-feeding by
carps on natural prey and cereals require at least two growing
seasons to reach marketable table-sizes (>1.5 e2 kg) under
temperate conditions in Western and Central Europe (G
al et al.,
2016;Pechar, 2000). Unlike Asia (e.g. Indian major carp produc-
tion, up to 10e11 tons ha
1
year
1
(ICAR, 2011)), the carp farming in
Europe is occurring at far lesser intensity, with state and/or EU
ratied environmental legislations in place (reviewed in OHagan
et al., 2017).
Unlike Asian shponds, fertilizing shponds in Europe have
already different levels of restrictions among different countries
(G
al et al., 2015), e.g. prohibited in the Czech Republic. Most carp
farmers therefore regard their pond sediment as the only fertilizer
they need and are anxious not to ush it out (Kn
osche et al., 2000;
Potu
z
ak et al., 2016), while some perform green manuring on dried
pond beds and later lling them (Hartman et al., 2015). This nar-
rows it down to a more regular practice i.e. supplementary feeding;
probably the only major, deliberateallochthonous nutrient source.
The leading role played by feed and feeding efciency on the
environmental impact of any aquaculture practice is well recog-
nized (Aubin et al., 2009;Henriksson et al., 2015;Papatryphon
et al., 2004). Likewise, a great deal for nutrient loading from carp
dominated systems depend on the choice and proportion of sup-
plementary feed used (Biermann and Geist, 2019;Jahan et al., 2002,
2003;Watanabe et al., 1999). Common carp (Cyprinus carpio) can
lose about 50e79% of N intake through metabolizable and faecal
losses (Kaushik, 1995;Roy et al., 2019). Apart from its natural prey,
carps lose quite a lot of dietary P (53e73% of dietary P intake) from
most of the articial feedstuffs (Hua and Bureau, 2010;Roy et al.,
2019), including cereals. Half of the excreted P from carps was re-
ported to be directly available for algal production (Lamarra, 1975),
probably corresponding to the fractions of ortho-phosphate which
is readily assimilated.
The present water directive of EU insists carp waters (waters for/
from cyprinid culture) to maintain 0.4 mg L
1
PO
4
and 1mgL
1
NH
4
(EU Directive, 2006/44/E Article 3 &5, Annex I). There have
been concerns surrounding the impacts of carp culture in shponds
on eutrophication of associated water bodies (reviewed in Roy
et al., 2019). It has resulted in arguments and lobbying between
environmentalists and carp farmers regarding shpond-
environment legislations (e.g. Czech Republic: Duras and Potu
z
ak,
2016,2019,Duras, 2019; Germany and Hungary: Kn
osche et al.,
2000; Poland: Kufel, 2012,Mazurkiewicz, 2009). Amidst these
arguments, even the supplementary feeding gets tagged as a
harmful substanceapplied to shponds (Duras and Potu
z
ak,
2019). Such stringent measures or presumptions restricting the
intensity of carp farming in European shponds, in order to reduce
environmental footprint, have impacts on commercial viability too.
The market prices of common carp have in fact come down
signicantly in most European countries (FAO Globesh, 2018;G
al
et al., 2015). Present farm-gate prices of carp in the Czech Republic
and Germany are ~2e2.5 Vkg
1
live weight (EUMOFA, 2016;
OHagan et al., 2017) or even lower (1.9 Vkg
1
live weight) in
Hungary (FAO Globesh, 2018). Although the concerns of envi-
ronmentalists are in good faith, however, being too harsh on carp
farming without clariedknowledge is unfair.
In order that sustainable management strategies in aquaculture
be based on environmental impact analyses, life cycle assessment
(LCA) often is the rst choice (Aubin et al., 2009;Mungkung et al.,
2013;Philis et al., 2019). Albeit the advantages (Biermann and Geist,
2019), ambiguities in inventory creation, methodological incom-
pleteness and limited comparability across production systems or
studies exists (reviewed in Philis et al., 2019, Biermann and Geist).
The supply chain of agriculture-livestock sector, for example cereals
supply chain, is also important in achieving cleaner production
goals. Novel approaches in supply chain assessment and inventory
management already exists (Duan et al., 2018;Hoseini Shekarabi
et al., 2019;Gharaei et al., 2019a,b,c,d). To the best of our knowl-
edge, the environmental impact of carp farming has been subject to
only three LCA case studies eIndonesian net cage system
(Mungkung et al., 2013), Indian carp polyculture system (Aubin
et al., 2011) and German shponds (Biermann and Geist, 2019).
These LCAs were more focused on percentage contributionof
various management parameters towards multiple threat cate-
gories (e.g. climate change, eutrophication, toxicity, energy use,
etc.). Employing an alternative approach, we rather focused on
quantifying the key parameters itself (i.e. primary nutrients, N and
P) in the dominant pathway (feeding activity) of the core produc-
tion stage (shponds) driving a threat category (freshwater eutro-
phication). The LCA and supply chain concepts were beyond the
scope of our present, already extensive exercise.
In our present attempt, we have assessed the primary envi-
ronmental macronutrient (N and P) footprint of carp farming in
Czech Republic. By the term footprint, we imply nutrients excreted
(faecal and metabolic losses) into the aquatic environment by the
carps. The aim is to have an objective assessment of eutrophication
incriminated by carp farming in the region. The objectives were to
assess e(a) nutrient footprint of carps feeding on supplementary
feed (cereals) and natural prey in shponds, employing different
methodologies; (b) nutrient footprint of carp production in com-
parison to EU crop and livestock production; (c) nutrient utilization
efciencies by carps in shponds and comparison with other EU
food production sectors; (d) autochthonous nutrient removal by
carps; (e) environmental cost burden worth of nutrient footprint in
contrast to total ecosystem services offered by carp production in
shponds; (f) required production intensity in shponds to
neutralize nutrient footprint and its practicality; (g) trade-offs be-
tween good growth (optimum digestible nutrient supply) and
reduced footprint. We have further extrapolated our ndings onto
the production scenarios of Germany, Hungary, Poland and Russian
Federation to generate a comprehensive picture of the central-
eastern European region (CEER) ea complimentary t to existing
assessments on EU crop-livestock sectors (Buckwell and Nadeu,
2016,Csatho et al., 2007, Gerber al. 2014, Kronvang et al., 2007,
Leip et al., 2011,2014,2015,Richards and Dawson, 2008,Rosendorf
et al., 2016,van Dijk et al., 2016,Velthof et al., 2007). The mana-
gerial implication of the present study is discussed at the end.
Abbreviations
FCR Food conversion ratio (¼dietary intake biomass
gain) used in relative sense (in the presence of
other food component in shponds i.e. natural
food or cereals)
FCR
cereals
Relative FCR of cereals in the presence of carps
natural food in shponds
FCR
natural prey
Relative FCR of carps natural food in the
presence of cereals as supplementary feed
CEER Central Eastern European region
EU European Union
NUE Nutrient Utilization Efciency
NUE
N
NUE of Nitrogen
NUE
P
NUE of Phosphorus
LCA Life Cycle Assessment
GHG EI Greenhouse gas Emission Intensity (kg CO
2
-
equivalent per kg consumable weight)
K. Roy et al. / Journal of Cleaner Production 270 (2020) 1222682
2. Materials and methods
2.1. Collection of baseline statistics for carp production
Carp production statistics (18460 tons from 41080 ha of sh-
ponds; yield 449.4 kg ha
1
) was obtained from CZ-Ryby (2019).
Relative feeding coefcient (i.e. relative food conversion ratio in the
presence of natural food) of cereals supporting carp production in
shponds of the region have been estimated at 2e2.5
(Woynarovich et al., 2010, Jan Mraz, IAPW FROV Ceske Budejovice e
unpublished data, Martin Oberle, LfL-Bayern Bavaria eunpublished
data). Collating higher nutrient richness and digestibility of carps
natural prey over cereals (Table 1), natural food was found to be
6e8 times superior in terms of digestible nutrient supply per unit
dry matter. Therefore, FCR of natural prey was back calculated from
standardized FCR of cereals and estimated at 0.3e0.4. Here, the
term FCRimplies food conversion ratio (¼dietary intake
biomass gain) in relative sense. FCR
cereals
imply FCR of cereals in the
presence of carps natural food in shponds. FCR
natural prey
imply
FCR of carps natural food in the presence of cereals as supple-
mentary feed.
In the absence of supplementary feeding with cereals (i.e.
exclusively natural production), the annual yield in temperate
Czech shponds (thermal cycle 6.9e26.8
C;
Rezní
ckov
a et al.,
2016;Kopp et al., 2016) is around 250e300 kg ha
1
(Pechar,
2000;Duras and Dziaman, 2010, Mraz eunpublished data). In
this case, absolute FCR of natural food was estimated at least ~0.7 to
fulll the optimum digestible nutrient supply for growing carps.
2.2. Assessment of nutrient availabilities from supplementary feed
(cereals) and natural food
Apparent digestibility of N and P of commonly used cereals in
Czech shponds (wheat, corn, triticale) and carps natural prey
(daphnia, chironomid larvae, cyclops) were determined, following
standard procedures (NRC, 2011;Glencross et al., 2007). Di-
gestibility trials were conducted in a 12 tank Guelph system (6
control þ6 treatment; 120 L capacity each; Cho and Slinger, 1979)
for facilitating passive collection of faeces from carps (Cyprinus
carpio) weighing 150e475 g (mixed assortment of sizes; 6e7kg
carp biomass per tank). Trials were conducted under species opti-
mum conditions: temperature 19e21
C, dissolved oxygen
>4mgL
1
, pH 6.8e7.3 and unionized ammonia <0.05 mg L
1
. The
procedures entailing experimental feed preparation, feeding, faeces
collection and sample processing have been detailed in supple-
mentary text. Apparent digestibility coefcients of N (ADC
N
) and P
(ADC
P
), both diet and ingredient level, were calculated following
the formula given in NRC (2011). All calculations were done on
100% dry matter basis. In total, the entire experiment lasted for 7
months.
2.3. Collection and use of reference metadata
From the online databases, literature metadata were compiled
for the following categories: (a) N:P balances, NUEs of EU
agriculture-livestock sectors (data from Buckwell and Nadeu, 2016,
Csatho et al., 2007, Gerber al. 2014, Kronvang et al., 2007,Leip et al.,
2011,2014,2015,Richards and Dawson, 2008,Rosendorf et al.,
2016,van Dijk et al., 2016,Velthof et al., 2007); (b) cost of
removing 1 kg N or P from wastewaters (freshwater origin) (data
from Bashar et al., 2018;Huang et al., 2015;Mangi, 2016;Mackay
et al., 2014;Molinos-Senante et al., 2011;Vinten et al., 2012); (c)
valuation of regulatory eco-services by shponds of CEER origin
(meta-analysed by Fr
elichov
a et al., 2014; Czech Republic), and; (d)
farm-gate prices of common carp, live-weight basis (EUMOFA,
2016;OHagan et al., 2017). All these metadata were used for
further comparison or calculation (indicated below).
3. Calculation
3.1. N and P losses from carps feeding in shponds
N and P losses from carps feeding in shponds involved the
following calculations in sequence: (a) total input of feed, dietary N
and P; (b) estimating digestible, metabolic and total losses; (c)
calculation of nutrient balances from diffused losses eapproach A;
(d) calculation of net nutrient balances from feed (cereals) losses e
approach B; (e) calculation of net nutrient balances from cumula-
tive losses eapproach C, and; (f) representative footprint merging
all approaches and comparison with other sectors. Considering the
space limitations, these sub-chapters are explained in the supple-
mentary text.
3.2. Nutrient utilization efciency and comparison with other
sectors
N and P retentions in carp were back calculated by assuming
2.88% N and 0.76% P content on whole body basis (Ramseyer, 2002;
Roy et al., 2019, Mraz et al. unpublished results). These values were
multiplied with harvested biomass of carp to estimate N and P
harvested. Harvested values were subtracted from total dietary N or
P (cereals and natural prey combined) and expressed in percentage
(NUE
N
, NUE
P
). For comparison, we used published estimates on
NUE
N
, NUE
P
from crop and livestock production sector(s) within EU
region.
3.3. Autochthonous nutrient extraction by carps
There is inherent complexity in determining nutrients of
autochthonous origin extracted by carps from shponds (Potu
z
ak
et al., 2016), especially in the presence allochthonous input like
Table 1
Results from the digestibility trials with common carp (data on dry matter basis).
Food Crude N (%) ADC
N
(%) Digestible N (g 100 g
1
) Crude P (%) ADC
P
(%) Digestible P (g 100 g
1
)
Corn 2.14 70.9 1.52 0.38 24 0.09
Triticale a2.5 37.8 0.95 0.36 1 e
Wheat b3.24 75.7 2.45 1 36 0.36
Average
cereals
2.62 61.5 1.61 0.58 20.3 0.12
Chironomid larvae b8.46 91.9 7.77 0.99 99 0.98
Cyclops b11.3 74.9 8.46 1.24 72.1 0.89
Daphnia b8.95 80.5 7.2 1.34 72.2 0.97
Average
natural prey
9.57 82.4 7.89 1.19 81.1 0.97
Skretting®Carpe-F 3.5 mm(commercial carp feed)
a
5.93 85.2 5.05 1.05 40.6 0.43
Intra-group comparison (cereals or natural prey): bComparatively good; aComparatively poor.
a
Control diet. Results given for reference purpose. ADC ¼Apparent digestibility coefcient.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 3
supplementary feeding. We attempted to grossly indicate the nu-
trients of autochthonous origin withdrawn by carps. The portion of
retained nutrients from natural prey in carp body was grossly
budgeted (in the absence of stable isotope approach). It was
calculated by subtracting total losses of natural prey origin from
total dietary intake (nutrient) of natural prey. The terms autoch-
thonous and allochthonous refer to nutrients either originating
from within the shponds or introduced to the shponds from
outside, respectively.
3.4. Environmental cost burden and ecosystem services of carp
production in shponds
With the existing water treatment technologies, cost of
removing 1 kg N or P from wastewaters (freshwater origin), were
meta-analysed. The inter-quartile ranges of costs were 3e5V
kg
1
N removed and 19e35 Vkg
1
P removed. These costs were
multiplied with calculated nutrient footprint and regarded as
environmental cost burden. Under ecosystem services offered,
following aspects were summed up: (a) non-production or regu-
latory services offered by shponds in Czech Republic (1257 V
ha
1
); (b) commercial production services offered by shponds
(~2e2.5 Vkg
1
live weight), and; (c) valuation of autochthonous
nutrient removed (cost mentioned above). All valuations were
made on per ha shpondbasis.
3.5. Neutral-footprint carp production scenario
The required cereals-based production intensity in shponds to
neutralize existing footprint to near-zerolevels was coined as
neutral footprintproduction. For its mathematical derivation,
median values between exclusively naturaland existingpro-
duction scenarios were calculated for certain variables, i.e. FCR
natural
prey
, FCR
cereals
, yield (kg ha
1
), NUE
N
and NUE
P
. Nutrient balances
from feeding within this median scenariowas calculated and
validated for sub- or near-zero values.
3.6. Trade-offs between nutrient supply, good growth and reduced
footprint
An exercise was done with different relevant combinations of
cereals and natural prey (FCR
cereals
0e4.3; FCR
natural prey
0.1e0.7)
covering exclusively naturalto completely cereals dominated
production scenarios. Digestible N and P (g kg
1
fed basis) from
cereals and natural prey were multiplied with their respective FCRs
and summed up for total diet. NRC (2011) recommendations on
optimum digestible nutrient requirement of common carp were
used as baseline, i.e. 49.6 g digestible N kg
1
of diet and 7 g
digestible P kg
1
of diet. The instances of FCR combinations which
successfully hit the target(i.e. fullled baseline) were demarcated
from the ones that failed. Multiple linear regression models were
generated to aid such budgeting.
Similar exercise was repeated with footprint (faecal losses in g
kg
1
diet basis) from cereals and natural prey under different FCR
combinations (same range as above). Complimentary contribution
curves of faecal footprint under different FCR combinations were
plotted in ggplot2 using linear tting (Wickham, 2016;R
Development Core Team, 2015). The FCRs at the intersection was
designated as trade-off point to reduce faecal footprint without
deviating from optimum digestible nutrient supply. By the term
trade-off, we imply a balanced compromise where we accept some
degree of disadvantage (reduced footprint) to retain a benet
(uninterrupted production), which otherwise are two incompatible
features.
3.7. Data application in Central and Eastern European Region
(CEER) production scenario
Values obtained on Czech carp production were upscaled and
applied for Germany, Hungary, Poland and Russian Federation to
derive gures representing Central and Eastern European Region
(CEER). The strategy is detailed in supplementary text. In addition
to the text above, infographics on the methodological framework
are provided in Supplementary Figs. S4eS5 for better clarity.
4. Results
4.1. Nutrient availabilities from cereals and natural prey
On dry matter basis, the average N and P contents in cereals
commonly used in Czech shponds (corn, triticale, wheat) is 2.62%
and 0.58%, respectively. Carps natural prey (chironomid larvae,
cyclops, daphnia) have much higher N (9.57%) and P (1.19%) con-
tents. Apparent digestibility of N in cereals and natural prey were
61.5% and 82.4%, respectively. Natural prey-N is therefore ~1.3 times
more digestible than cereal-N. Likewise, apparent digestibility of
natural prey-P (81.1%) is ~4 times superior to cereal-P which is only
20.3% digestible. The digestible nutrients offered by natural prey
(N: 7.89 g 100 g
1
;P:0.97g100g
1
)are~5e8 times higher
(p<0.05) than cereals (N: 1.61 g 100 g
1
;P:0.12g100g
1
).
Detailed results are summarized in Table 1.
4.2. N and P losses from carps feeding in shponds
4.2.1. Cereals
It was estimated about 36920e46150 tons of cereals
(~967.3e1209.1 tons N, 214.1e267.7 tons P) supported carp pro-
duction in Czech shponds (Table 2). Combining the global meta-
data and our digestibility results, the N and P digestibility of cereals
usually range between 61.5e71% and 20.3e25% respectively. It
implies 29e38.5% of cereal-N and 75e79.7% of cereal-P are not
digested by carps. Considering the metabolic N losses through gills
and urine, another 17e30% of N intake is lost. Faecal and metabolic
losses from feeding on cereals was estimated at 24.1e44.9 kg N and
8.7e11.6 kg P ton
1
of carp produced or, 10.8e20.2 kg N and
3.9e5.2 kg P ha
1
shpond. The N:P ratio of cereals derived losses is
~3:1e4:1 (Table 2).
4.2.2. Natural prey
About 5538e7384 tons of natural prey dry matter (~530e706.6
tons N, 65.9e87.9 tons P) was supposedly consumed by the carp
production in Czech shponds (Table 2). Due to lack of pre-existing
data on N and P digestibility of natural prey, only results obtained
from our digestibility trials were used. About 17.6% of natural prey-
N and 18.9% of natural prey-P are not digested by carps. Another
17e30% of N intake is lost as metabolic losses. Carps digestive
losses from grazing on natural prey was estimated at 9.9e18.2 kg N
and 0.7e0.9 kg P ton carp produced
1
or, 4.5e8.2 kg N and
0.3e0.4 kg P ha
1
shpond. The N:P ratio of natural prey derived
losses is ~14:1e20:1 (Table 2). Compared to cereals, the losses of
natural prey origin are far less and with better N:P ratio. If the sum
of losses from cereals and natural prey is considered, cereals has the
major share of total footprint (>70% of N and >90% of P footprint).
4.3. Nutrient footprint through the production cycle and
comparison with other sectors
Using multiple approaches, the nutrient balance from carps
feeding activity in shponds were calculated (Table 2). The spatial
footprint (footprint expressed per unit farmed area) of common
K. Roy et al. / Journal of Cleaner Production 270 (2020) 1222684
carp production in Czech shponds was estimated at
7.08e13.45 kg N and 2.65e3.35 kg P ha
1
(equivalent to
15.8e29.9 kg N and 5.9e7.5 kg P ton
1
of carp produced). In terms
of N footprint, carp production in European shponds appear ~4e6
times less burdening than other food production sectors. Regarding
P, carp production is ~1.5e2.4 times less burdening than other
sectors (Fig. 1a and b).
4.4. Nutrient utilization efciency and comparison with other
sectors
Comparing the total nutrient input (cereals þnatural prey) with
output through harvested carp biomass (12.9 kg N and 3.4 kg P ha
1
shpond), NUE
N
in shponds was estimated at 27.7e35.4% and
NUE
P
at 39.1e50% of dietary intakes. In case of completely natural
carp production (input from natural prey: ~20.7 kg N and ~2.6 kg P
ha
1
shpond; output carp biomass: ~8.6 kg N and ~2.3 kg P ha
1
shpond), the NUE
N
and NUE
P
are ~41.5% and ~88% respectively. A
marked improvement in NUE
P
is evident. Inter-sectoral comparison
of NUEs, with cereal-fed (present regime), fully natural and neutral
footprint production scenarios are depicted in Fig. 2a, b.
4.5. Autochthonous nutrient extraction by carps
Under the present production regime, about 18.8e20.1 kg N and
2.9e3.9 kg P of autochthonous origin (i.e. from live prey) is with-
drawn per ton of carp produced. It is equivalent to 8.4e9 kg N and
1.3 e1.7 k g P ha
1
of shponds. It should be noted that despite this
nutrient removal, the above-mentioned nutrient footprint is a spin-
off product of the production cycle. Hence, it should not be double
subtracted while comparing. If the production scenario is assumed
exclusively natural, autochthonous nutrient removal is ~19.2 kg N
and ~5.1 kg P ton
1
of carp produced, or, ~8.6 kg N and ~2.3 kg P
ha
1
of shponds. In this case no nutrient footprint occurs, and the
autochthonous nutrients removed by carps contributes to positive
ecosystem service. The present cereal-based production regime
seems only ~2.2 times or ~1.5 times less efcient in terms of
autochthonous N and P removal respectively, compared to natural
production.
4.6. Environmental cost burden and ecosystem services of carp
production in shponds
The environmental cost burden, under the present production
regime, was estimated at ~72e184 Vha
1
. Whereas, ecosystem
services offered by carp production and shponds amount to
~2206e2485 Vha
1
. It is obvious that environmental cost
burden ecosystem services. Environmental cost burden of carp
production amounts to <10% of its positive services to the envi-
ronment and commerce combined. Present carp production regime
is already inclined towards positive ecosystem services with net
worthof 2134e2300 Vha
1
. Under completely natural carp pro-
duction, with zero environmental cost burden, the service amounts
to ~1926e2130 Vha
1
. It is apparent that cereals-based carp pro-
duction delivers ~8e10% higher services than completely natural
production. This difference is driven by saleable amount of carp
from shponds, realized by the application of cereals. A compara-
tive and self-explanatory account has been depicted in Fig. 3 and
Fig. S7 respectively.
4.7. Assessment of neutral footprint carp production scenario
Neutralizing existing footprint to negligible levels might require
FCR
cereals
1e1.3 and FCR
natural prey
: 0.5e0.6 with a yield limitation of
374.7 kg ha
1
. In this scenario, NUE
N
and NUE
P
is expected to be in
the range of 34.6e38.5% and 63.6e69% respectively. The nutrient
footprint under such circumstances is estimated to be 0.8
(removal) to 2.4 kg N ha
1
shpond and 0.2 (negligible) to 0.5 kg P
ha
1
shpond. Although theoretically proposed, some application
bottlenecks might render its practicality questionable (claried
later).
4.8. Trade-offs between nutrient supply, good growth and reduced
footprint
4.8.1. Digestible nutrient supply
Digestible N requirement is easily met under semi-intensive
rearing conditions. However, meeting the digestible P demand
remains a concern under low natural prey availability emight be
even inadequate (red zones; Tabl e 3). Increasing supplementary
feed inputs (cereals, from FCR 2 to 2.5) under low support from
Table 2
Nutrient footprint from natural and supplementary feeding supporting 18460 tons of common carp production from 41080 ha of shponds (yield 449.4 kg ha
1
) in Czech
Republic.
Cereals (FCR 2e2.5) Natural food (FCR 0.3e0.4)
Dietary input
Requirement: 36920e46150 tons (dry matter) Requirement: 5538e7384 tons (dry matter)
Avg. N: 2.62% and P: 0.58% (dry matter) Avg. N: 9.57% and P: 1.19% (dry matter)
52.4e65.5 kg N ton carp
1
23.5e29.4 kg N ha
1
shpond
28.7e38.3 kg N ton carp
1
12.9e17.2 kg N ha
1
shpond
11.6e14.5 kg P ton carp
1
5.2e6.5 kg P ha
1
shpond
3.6e4.8 kg P ton carp
1
1.6e2.1 kg P ha
1
shpond
Faecal and metabolic losses
Faecal losses: 29e38.5% N; 75e79.7% P Faecal losses: 17.6% N; 18.9% P
Metabolic losses: 17e30% of N intake Metabolic losses: 17e30% of N intake
24.1e44.9 kg N ton carp
1
10.8e20.2 kg N ha
1
shpond
9.9e18.2 kg N ton carp produced
1
4.5e8.2 kg N ha
1
shpond
8.7e11.6 kg P ton carp
1
3.9e5.2 kg P ha
1
shpond
0.7e0.9 kg P ton carp produced
1
0.3e0.4 kg P ha
1
shpond
N:P ~3:1e4:1 N:P ~14:1e20:1
Spatial footprint on environment (per ha shpond)
Approach A (diffused) Approach B (allochthonous) Approach C (cumulative) Representative footprint (merged)
7.6e14.2 kg N ha
1
2.4e11.2 kg N ha
1
6.9e19.3 kg N ha
1
7.08e13.45 kg N ha
1
2.1e2.8 kg P ha
1
2.6e3.5 kg P ha
1
2.9e3.9 kg P ha
1
2.65e3.35 kg P ha
1
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 5
natural prey (FCR
natural prey
:0.3) does not necessarily help. The
nutritionally fullling combinations of relative FCRs have been
identied as green zonesin Ta ble 3 . To reduce the use of cereals
(by 15% to 25%) in shponds, the minimum support from
natural prey must be pushed by þ0.1 units (or, þ25%), i.e.
FCR
natural prey
should be 0.4 for supporting carp production
(modied scenario; Table 3). Although this 25% (þ0.1 FCR) in-
crease of dependency on natural prey appears theoretically
promising, it is difcult practically (discussed below). Multiple
linear models for calibrating digestible nutrient supply in sh-
ponds have been generated (Table 3).
4.8.2. Footprint of fecal origin (excluding uneaten feed)
Faecal nutrient losses progressively increase with relative in-
crease in FCR
cereals
while decrease with relative increase in FCR
na-
tural prey
(Fig. 4). It means higher dependency on cereals has
Fig 1. (a, b): Spatial nitrogen (a) and phosphorus (b) footprints of different farming sectors within EU or Central Eastern European Region (CEER). Data from Buckwell and Nadeu
(2016),van Dijk et al. (2016),Rosendorf et al. (2016),Leip et al. (2015),Richards and Dawson (2008),Csath
o et al. (2007),Kronvang et al. (2007),Velthof et al. (2007) and present
study. Carp production in shponds, in general, have the least nutrient burdens to environment than any other food production sector in Europe. Nutrient footprint below zero
indicates nutrient removal from shpond ecosystem.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 1222686
inevitable consequences on magnication of nutrient footprint;
indicated by the red line in Fig. 4a, b. Increased reliance on natural
food have positive environmental consequences; blue line in
Fig. 4a, b. The trade-off FCRs for minimizing footprint and yet
supplying optimum digestible nutrient were identied at FCR
cereals
2.2 and FCR
natural prey
0.35 (Fig. 4). Compliance to these relative
FCR recommendations may result in ~10% reduction in existing
footprint without compromising growth (digestible nutrient sup-
ply) or production (discussed below).
4.9. Central and Eastern European Region (CEER) carp production
scenario
Data on nutrient footprint, nutrient removal, eco-cost burden
and eco-services of carp production in Europe are provided in
Table 4. The prole is based on ve major European producers of
common carp (Czech Republic, Poland, Hungary, Germany and
Russian Federation) producing >72% of the total carp in Europe. The
yield, nutrient footprint and removal, eco-burden and services are
Fig 2. (a, b): Animal or plant level nutrient utilization efciencies for nitrogen (a) and phosphorus (b) of different farming components within EU. Data from Buckwell and Nadeu
(2016),Gerber et al. (2014),Leip et al. (2011) and present study. In terms of NUE
N
and NUE
P
, common carp is superior than EU27 livestock or EU27 crop and livestock average but
inferior to EU27 crop sector average.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 7
comparable among Czech Republic, Germany, Hungary and Poland
(p>0.05); Germany being slightly on a lower side than others.
Russian Federation has signicantly higher gures in all aspects
(p<0.05).
With a yield of 488.8 kg carp ha
1
, the N and P footprint from
CEER is currently estimated at ~7.7e14.6 kg N and ~2.9e3.7 kg P
ha
1
respectively. This amounts to ~19.7e50.9 million Vof eco-cost
burden in the region. The autochthonous N (8e9.2 kg ha
1
) and P
(1.4e1. 6 kg h a
1
) bioremediated by carps from shponds in CEER,
coupled with production value and regulatory services of shponds
is worth ~578.9e656.2 million Von regional scale (Table 4). The
European country level averages of spatial footprint are
~9.4e10.8 kg N and ~2.7e3.2 kg P ha
1
with an average eco-cost
burden of ~3.5e5.3 million V. The autochthonous nutrient
Table 3
Digestible nutrient supply (g kg
1
diet) from cereals (supplementary feed) and natural prey under different FCR (relative feeding coefcient) combinations for optimum carp
growth in shponds.
Fig. 3. Comparative account of ecosystem services (above red line) and environmental cost burden (below red line): Carp production in shponds has far greater positive services
compared to miniscule negative effect of supplementary feeding through cereals. Crop and livestock sectors in EU or CEER (Central Eastern European Region) have greater
environmental cost burdens than carp farming. (For interpretation of the references to colour in this gure legend, the reader is referred to the Web version of this article.)
K. Roy et al. / Journal of Cleaner Production 270 (2020) 1222688
removal (average 9.2e9.8 kg N and 1.4e1.9 k g P ha
1
), coupled with
production value (average ~1042.9 Vha
1
) and regulatory services
by shponds (~1257 Vha
1
) is worth ~74.5e100.6 million Von
national scale (Table 4). The positive services of carp farming in
European shponds is many folds higher (~13e29 times) than any
cost burden through nutrient footprint (Figs. 5 and 6).
5. Discussion
5.1. Nutrient availabilities from cereals and natural prey
The apparent protein (i.e. N) digestibility of various cereals by
common carp have been well studied over last six decades (Roy
et al., 2019), whereas data are sparse as regards to the availability
of P. The existing studies have been listed in supplementary text.
From the global metadata (Roy et al., 2019), the inter-quartile range
(IR) of N digestibility for corn and wheat is 74e80% and 62e92%
respectively. No data on P digestibility of corn and wheat for
common carp was encountered in the reviewed literature (Roy
et al., 2019). The present results are possibly the rst ones. To the
best of our knowledge, N and P digestibility of triticale (a hybrid
between corn and wheat) by Cyprinus carpio is reported here for
the rst time. Generally, 71e93% of cereals-N and 25e57% (IRs) of
cereals-P are digested by common carp (Roy et al., 2019). Our di-
gestibility results agree with this general range but near the lower
end of IRs (see supplementary text). The reason behind the poor P
digestibility is predominantly phytate bound P fractions in cereals
that are indigestible by carps (Hua and Bureau, 2010). N di-
gestibility of cereals is moderate to good in nature, depending on
their amino acid (AA) prole. Deciencies in certain AAs render
lower N digestibility (Kaushik, 1995;Nwanna et al., 2012;Schwarz
et al., 1998).
To the best of our knowledge (Roy et al., 2019), digestibility of
natural preys (chironomid larvae, cyclops and daphnia) by C. carpio
are reported here for the rst time. No prior data existed on
digestible N and P supply, although their superior nutrient contents
have been discussed before (Bogut et al., 2007;Steffens, 1986).
Here, we have observed ~5e8 times higher digestible N, P supply
from natural prey than cereals.
5.2. N and P losses from carps feeding in shponds
Within Europe, especially from the Central region, only a
handful of publishedestimates on carp shpond nutrient balances
exists: e.g. Austria (Kainz, 1985), Czech Republic (Duras et al., 2018;
Potu
z
ak et al., 2016;Prikryl, 1983), Germany (Kn
osche et al., 2000)
and Hungary (G
al et al., 2016;Kn
osche et al., 2000;Ol
ah et al.,
1994). From these studies it could be summarized that: (a)
average balance of N is ~23 kg ha
1
or ~24 kg ton
1
of carp pro-
duced; (b) maximum balance of P is ~6.7 kg ha
1
or ~2.7 kg ton
1
of
Fig 4. (a, b): Complimentary footprint (faecal) curve under relative proportions of cereals and natural food in shponds. Point of inter-section denote trade-off FCRs (cereals 2.2
and natural prey 0.35) to reduce faecal nutrient losses in shponds (FaecFootp.N, FaecFootp.P; in g kg
1
diet) without compromising optimum digestible nutrient supply for good
growth. Red line and blue line correspond relative feed efciency of cereals (supplementary feed) and natural prey, respectively. Nutrient footprint from feeding increases with
relative increase in cereals input and relative decrease in natural food availability.
Table 4
Environmental footprint and bio-remediation services of carp production in Europe. Prole based on major European producers of common carp.
Country/Region
a
Yield (kg
ha
1
)
Footprint N (kg
ha
1
)
Footprint P (kg
ha
1
)
N removed (kg
ha
1
)
P removed (kg
ha
1
)
Eco-burden (million
V)
b
Eco-service (million
V)
b
Czech Republic 449.4 7.1e13.4 2.7e3.4 8.4e9 1.3e1.8 2.9e7.6 90.6e102.2
Germany 250 4e7.5 1.5e1.9 4.7e5 0.7e1 1.6e4.1 71.4e77.7
Hungary 470.8 7.4e14.1 2.8e3.5 8.9e9.5 1.4e1.8 2e5 58.5e66.2
Poland 410 6.5e12.3 2.4e3.1 7.7e8.2 1.2e1.6 2.9e7.5 94.9e106.3
Russia 638.8 10.1e19.1 3.8e4.8 12e12.8 1.9e2.5 10.3e26.6 263.5e303.9
Central Eastern European
Region
c
488.8 7.7e14.6 2.9e3.7 9.2e9.8 1.4e1.9 19.7e50.9 578.9e656.2
Country average
d
(European) 9.4e10.8 2.7e3.2 8e9.2 1.4e1.6 3.5e5.3 74.5e100.6
a
Carp Production/carp shpond area (as of 2017; in parenthesis): Czech Republic (18460 tons/41080 ha), Germany (10000 tons/40000 ha), Hungary (12240 tons/26000 ha),
Poland (18325 tons/44700 ha) and Russia (64587 tons/101100 ha).
b
Eco-burden: cost burden due to nutrient footprint. Eco-service: regulatory services of shponds, autochthonous nutrients bioremediated by carp, farm-gate sale value of
harvested carps. All values in million Veon national scale.
c
Derived from total carp production (123612 tons) and total carp pond area (252880 ha) in the region (sum of countries).
d
Inter-quartile range of medians. Median value derived from the minima-maxima span of top ve common carp producing countries in Europe.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 9
carp produced; and, (c) shponds have special benets of acting as
a sink for P, trapping ~0.5e78 kg P ha
1
(average ~34 kg P ha
1
).
Although most of them emphasized the non-polluting nature of
carp production in shponds through mass balance approach, no
attempt pin-pointed the nutrients left behind by the growing carps
through their feeding activity per production cycle. The most dy-
namic uctuation of nutrients in shponds is perhaps through the
type and quantity of food consumed (Biermann and Geist, 2019;
Kn
osche et al., 2000;Pechar, 2000;Watanabe et al., 1999). N or P
balance of shponds beyond carps excretory losses from feeding
Fig. 5. Breakdown (million V) of different eco-services associated with carp production in shponds on national scale. Figure depicts national scale average from top 5 producers in
Europe (Russian Federation, Czech Republic, Poland, Hungary and Germany; contributing >70% production in Europe). Per hectare averages of top producers: Nutrient bio-
remediated by carp worth ~75.3 Vha
1
, nutrient footprint of production (negative service) worth ~120.8 Vha
1
, production value of harvested biomass worth ~1042.9 Vha
1
and
regulatory ecosystem services by shponds worth ~1257 Vha
1
.
Fig. 6. Worth of positive (right of dotted line) and negative (left) ecosystem services from carp production in shponds on national/regional scale. On country scales, Czech Republic
and Poland almost have 100 million Vof total services. Scale for comparison: total budget of EU spent on aquaculture during 20 00e2014 amounts to 1170 million V(Guillen et al.,
2019), 50% of which appears to be intangibly paid back bycarp production alone in CEER shponds per production cycle. Assuming 5 carp production cycles during 20 00e2014, carp
aquaculture alonemight have intangibly paid back ~2.9 billion Vwhich is 2.5 times over the invested budget.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 12226810
on natural prey and cereals (i.e. beyond our estimated footprint),
might have been the nutrients received through inow water or
catchment fertilization. The present work highlights this over-
looked interference in most shpond nutrient budgeting results.
Potu
z
ak et al. (2016) earlier validated the results derived
through the traditional methodology i.e. mass balance equations
between input and output of shponds. They demonstrated mass
balancedresults when validated under practical conditions seldom
make any sense. Alternative nutrient budgeting methods more
appropriate for Central European shponds were proposed (Hejzlar
et al., 2006;Potu
z
ak et al., 2016). Our results, if compared with the
mass-balancedresults, appears to be on a conservative side;
probably more realistic. Interestingly, our results are in close
agreement with an independent LCA by Biermann and Geist (2019)
on conventional and organic carp farming in Germany. The foot-
print from carp and feed combined was estimated ~10.5e50.5 kg N
and 5.7e6.3 kg P ton
1
of carp produced (recalculated from
Biermann and Geist, 2019); reinforcing our ndings.
5.3. Nutrient footprint through the production cycle and
comparison with other sectors
The EU crop and livestock (terrestrial) production sectors,
together, have spatial footprints in the range of 32e80 kg N and
4e8kgPha
1
farming area (Buckwell and Nadeu, 2016;Csatho
et al., 2007;Kronvang et al., 2007;Leip et al., 2015;Richards and
Dawson, 2008;Rosendorf et al., 2016;van Dijk et al., 2016,
Velthof et al., 2007). Hence, the spatial footprint of European
agriculture and livestock production is at least 1.5 times (for P) to 4
times (for N) higher than shpond-based, cereals-fed carp pro-
duction (European average: 9.9e11.4 kg N ha
1
; 2.2e2.6 kg P ha
1
).
Linking the estimated footprint with existing observations on
nutrient trapping by shponds (e.g. outow water-P <inow
water-P; G
al et al., 2016;Kn
osche et al., 2000;Potu
z
ak et al., 2016;
V
seti
ckov
a et al., 2012), we suspect the quantied footprint might
not always end-up enriching downstream waters. Long term water-
residence period is known to precipitate P into shpond sediments
(Hejzlar et al., 2006;Potu
z
ak et al., 2016), only a part of which is
released during harvesting through sludge (Duras et al., 2018;
Kn
osche et al., 2000;Potu
z
ak et al., 2016). It can be avoided, pro-
vided careful harvesting measures are adopted (Kn
osche et al.,
2000;Potu
z
ak et al., 2016).
We have further hinted a neutral footprint production intensity
in shponds, following which, the commercial interests of prot-
ablecarp production may falter edespite fullling greener-goals.
Downscaling the existing production to neutralor naturalmodes
may reduce earning by at least 170 Vha
1
or 223 Vha
1
respectively. This view, from environmentalists perspective, is a
traditional argument soldby the producers. Present production
regime, with still intactcommercial interests, is close to the
neutral footprint zone (Fig. 1a and b). However, compliance to the
trade-off FCRs (discussed below) and better pond management
practices (listed in supplementary text; Woynarovich et al., 2011)is
recommended. Present supplementary feeding provisions in sh-
ponds for supporting production should not be incriminated as an
anthropogenic driver of eutrophication.
Beyond eutrophication, two additional analyses on green-
house gas emission (e.g. CO
2
-equivalent and CH
4
) are presented
for additional clarity: (a) carbon emission from European carp
production in contrast to EU livestock sectors (illustrated in
Fig. 7), and; (b) methane emission from Czech shponds in
contrast to Asian carp ponds, Czech agricultural farms and live-
stock units (Fig. S6). The greenhouse gas emission intensity (GHG
EI) of EU livestock products (range 5e28 kg CO
2
-e, average
15.6 kg CO
2
-e kg
1
consumable weight) appear much higher than
farmed carp (2.9e4kgCO
2
-e kg
1
consumable weight) (Fig. 7).
Overall, the results reinforce European carp farming in shponds
as relatively cleanerway of production than other food
Fig. 7. GHG EI (kg CO
2
-equivalent per kg consumable weight) of European livestock produce in comparison with farmed carp. Maximum GHG EI of carp production is ~4 times less
than the average GHG EI of livestock sector (big/small ruminants, poultry). Carp farming in shponds is cleaner than most terrestrial animal farming. Carbon emission of EU/CEER
carp production was recalculated from dataset in MacLeod et al. (2019), then corrected with slaughter yield range for common carp (Prchal et al., 2018) to arrive at carp level GHG EI
values. For inter-sectoral comparison, data were taken from Weiss and Leip (2012).
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 11
production sectors.
5.4. Nutrient utilization efciency (NUE) and comparison with
other sectors
Under controlled conditions and with good quality protein diet,
common carp may retain up to ~50% of dietary N intake (Kaushik,
1980,1995;Roy et al., 2019). Metabolic losses (as soluble NH
4
eN),
predominantly through branchial pathway and little through
urine, are the major N losses in carps (Kaushik, 1980). In Czech
shponds, carps feeding on natural prey and cereals overall have
mediocre NUE
N
(up to 36% of dietary N intake). This might be
attributed to endogenous obligatory losses (NRC, 2011) to meet
energy expenditure, especially during survival through the ice-
covered winter months (90e120 days), in the absence of
adequate food. This is a situation unlike experimental or indoor
aquaculture systems where optimum temperature is maintained
with uninterrupted food supply. Carps even suspended feeding in
our indoor systems when water temperature dropped below 13
C.
Concerning P, suspended losses through faeces remains the most
dominant pathway (Kaushik, 1995;Roy et al., 2019). Present esti-
mates indicate ~50% of dietary P intake are likely retained by the
carps in Czech shponds; little better than NUE
N
. Carps excrete
more P in already high P environment (Chumchal and Drenner,
2004); a phenomenon which might coincide with spring thaw-
ing (and blooming) of shponds. During late spring to summer,
Czech shponds are known to release the highest amount of P
from sediments due to internal loading (Pokorný and Hauser,
2002;Vystavna et al., 2017).
The EU livestock sector (dairy cattle, beef cattle, pigs, poultry)
has animal level NUE
N
and NUE
P
in the range of 4e62% (average
18% ) an d 14e60% (average 29%) respectively (Buckwell and
Nadeu, 2016;Gerber et al., 2014;Leip et al., 2011). Hence, the
average NUEs of EU livestock sector appears 1.5e1.7 times infe-
rior than cereals based common carp production in European
shponds. Plant level NUE
N
and NUE
P
in the EU crop sector is
45e76% and 70% respectively (Buckwell and Nadeu, 2016); su-
perior to both livestock and carp production. With increasing
reliance on natural prey and decreasing production intensity
(existing /neutral footprint /natural regime), a progressive
improvement in NUE
P
has been predicted. In fact, the achievable
NUE
P
for common carp under neutral or natural production
regime are comparable or superior than the maximum NUE
P
of
crop and livestock sectors (Fig. 2a and b). Hence, presumptions
surrounding inferior NUEs of common carp, at animal level,
should be reconsidered; a lot depends on man-made choices.
5.5. Autochthonous nutrient extraction by carps
Our present estimate highlights the amount of autochthonous
nutrients carp extract from shponds through retention in body
(European average: 8e9.2 kg N and 1.4e1.6 k g P ha
1
). Like in the
case of footprint, our estimate of extracted nutrients is also on
conservative side compared to mass balancedresults (explained in
supplementary text). In terms of autochthonous nutrient extrac-
tion, present production regime is only ~1.5e2.2 times less efcient
than natural carp production. A more precise estimation would
require stable-isotopes approach; conveniently for N but difcult
for P. Nonetheless, greater retention of dietary N and P by farmed
sh is the key to balance aquaculture and environmental sustain-
ability goals (Rerat and Kaushik, 1995).
5.6. Environmental cost burden and ecosystem services of carp
production in shponds
Carp production in European shponds has been qualitatively
attributed to various positive services (Szücs et al., 2007;Bekeand
Varadi, 2007,Popp et al., 2019). Ecosystem services include ood
control, biomass production, nutrient remediation, biodiversity
support, groundwater recharge, oxygen production, micro-climate
regulation, carbon sequestration, aesthetics, etc. (Pokorný and
Hauser, 2002,Popp et al., 2019). Even the maximum production
service (up to ~1123 Vha
1
) comes after average eco-service (1257
Vha
1
;Fr
elichov
a et al., 2014) offered by regional shponds. In
addition, the production benet(þ298.8e373.5 Vha
1
) over nat-
ural yields due to use of cereals (as supplementary feed) outweighs
the little environmental cost burden caused (72e184 Vha
1
). This
advantage (Fig. S7) only applies given that weed sh biomass does
not select-out mature stages of zooplankton (natural prey) and
result in their population collapse (Musil et al., 2014;Zemanov
a
et al., 2019).
In the Czech Republic, present carp production regime offers
positive services of net worth ~2134e2300 Vha
1
(European
average: ~2375 Vha
1
); almost 100 million Von country scale. On
regional scale (CEER), total net worth of services is at least ~579
million V. If we consider the total budget of EU spent on aqua-
culture (1.17 billion V) during 2000e2014 (Guillen et al., 2019),
carp production in CEER shponds appears to have intangibly paid
back half of it per production cycle. Assuming 5 production cycles
(average 3 years per cycle; G
al et al., 2016;Pechar, 2000)during
the EU investment period (2000e2014), carp aquaculture alone
might have intangibly paid back ~2.9 billion Vi.e. ~2.5 times over
the invested budget. The positive services of carp farming in Eu-
ropean shpondsismanyfoldshigher(~13e29 times) than any
cost burden caused through nutrient footprint; little-bad
compared to the greater-good. This situation may be reversed to
greater-bad, lesser-good, losing >1118 Vha
1
or >56.5 million V
worth of services in CEER, if production regime is adjusted to
purely environmentalistsinterests (explained in supplementary
text).
5.7. Trade-offs between nutrient supply, good growth and reduced
footprint
Over the last four decades in Europe, there have been reports
alleging carp production in shponds as polluting and studies not
corroborating such allegations (listed in supplementary text;
reviewed in Roy et al., 2019). From a nutritional point of view, the
5e8 times superior digestible nutrient supply of natural prey over
cereals is not as straightforward as it seems. For example e
digestible N or P in one corn grain kernel (weighing ~0.38 g) is
available from ~0.05 to 0.08 g natural prey dry matter, but in sh-
ponds, it is equivalent to ~0.38e0.6 g natural prey biomass (wet
weight) roughly amounting to ~1230e1969 Daphnids or ~258e414
Chironomids (data from Bezmaternykh and Shcherbina, 2015;
Rezní
ckov
a et al., 2016,Sim
ci
c and Brancelj, 1997). One must ima-
gine the differences in energy allocation by carps in fetching one
static corn grain versus ltering equivalent numbers of active nat-
ural prey(s) in shponds. Cereals itself are rich and easy source of
digestible energy for carps (~2759.4 kcal kg
1
; our data) having an
energy prole slightly below their optimum requirement
(~3200 kcal kg
1
diet; NRC (2011)). On the other hand, production
solely on natural food has its own limitations. High value proteins
or lipids in natural prey, in the absence of cereals, are utilized for
energy rather than acting as building blocks for biomass gain
(Füllner, 2015). Here, the importance and role of cereals must be
recognized before including it in legislative discussions concerning
K. Roy et al. / Journal of Cleaner Production 270 (2020) 12226812
shpond environment (e.g. Czech Republic, Duras and Potu
z
ak,
2019). Importance of a good balance between natural food avail-
ability, supplementary feed application and nutrient footprint is
discussed below.
5.8. Managerial implications
Conclusions from previous life cycle assessments (LCAs)
highlight the feed and feeding efciency as fundamental to the
environmental impact of most aquaculture production systems
(e.g. Aubin et al., 2009;Biermann and Geist, 2019;Henriksson
et al., 2015;Mungkung et al., 2013;Papatryphon et al., 2004).
In a recent LCA assessment on German carp production in sh-
ponds (Biermann and Geist, 2019), feed contributed almost
unanimously to the impact category: eutrophication. The feed
types and amounts were proposed as point-of-action to improve
environmental sustainability of carp production atop other pa-
rameters. Any reduction in supplementary feeding alone greatly
lowers the freshwater eutrophication threat scenario posed by
shpond efuents (Biermann and Geist, 2019). Here, using an
alternative approach, we highlighted the same and quantied it.
To the best of our knowledge, this is the rstdata-driveneffortto
demarcate possible trade-offs in relative FCR combinations
(FCR
cereals
and FCR
natural prey
) for balancing environmental and
commercial goals of carp production.
The existing feeding regimen (FCR
cereals
2e2.5; FCR
natural prey
0.3e0.4) in European shponds already has its own bottlenecks;
detailed in the supplementary text. On both sides of the pro-
posed trade-off FCRs, it is either forcing farmers to reduce carp
production (e.g. maintaining FCR
natural prey
of 0.5 in shponds), or
inadequate supply of digestible nutrients for carpsoptimum
growth (e.g. if FCR
natural prey
is below 0.3, increasing cereals will
only cause footprint, not production). In the former case, at least
eco-subsidies should be offered to the farmers for their envi-
ronmental contribution. In the latter case, better supplementary
feed i.e. options beyond cereals should be availed (discussed
below). In the present study, we have mostly dealt with N while
discussing about protein. Fish need all 20 amino acids in
adequate quantities for protein growth (Kaushik, 1995;Rerat and
Kaushik, 1995). Cereals alone under low natural food availability
cannot provide that. Poor protein quality or amino acid prole of
carpsdietinshponds, caused by lower natural food availability
(i.e. abundant, high-quality protein) and excess cereals applica-
tion (i.e. scarce, low-quality protein), can aggravate metabolic N
losses up to 46.7e58.6% of dietary N intake (Roy et al., 2019). This
will most likely manifest into lower NUE
N
and higher N footprint
than presently estimated. In this situation, both N and P might be
of equal concern.
5.9. Future suggestions
Feeding management decisions in European carp farming
should involve e(a) further LCAs of arable cereals (Biermann and
Geist, 2019), including supply chain concepts (mentioned above);
(b) efforts toward lowering the overall FCR (Mungkung et al.,
2013;Biermann and Geist, 2019, present study) for improving
environmental performance; (c) validate our proposed trade-off
FCRs under practical conditions; (d) calibrate the stocking den-
sities (lower carp heads feeding on natural food) for reducing
existing footprint without compromising production; (e)
changing frequency, timing and dosages of feed application
depending on environmental conditions (Roy et al., 2019); (f)
supplementing the supplementary feedunder low natural food
availability ee.g. use of commercial carp feed (not cereals at
critically low natural food availability), partial replacement of
cereals with pulses-legumes having ~2.7 times higher digestible
P, or, brewery wastes offering ~4e5 times higher digestible P
than parent cereals (Roy et al., 2019, Vlastimil Stejskal, JCU-FROV
Ceske Budejovice, personal communication.). If reduced produc-
tion intensity is still imposed, at least the farmers should be
compensated with eco-subsidiesfor their environmental
contribution. To some extent, this would offset their decreased
farm-gate income.
6. Conclusion
The present study revealed that carp production in shponds
has the least nutrient burdens to environment compared to other
food production sectors in Europe. Existing feed provisioning in
carp ponds and production intensity cannot thus be considered
as a pollution causing activity. Focus should be on actual man-
agement of the shponds. The ecosystem and production ser-
vices offered by carp farming in shponds have immense societal
and economic advantages. Majority of nutrient footprint from
carps feeding activity is contributed by supplementary feeding
with cereals. Monetary benet of improved production over
natural yields, by using cereals, out-weighs the slightly increased
environmental burden caused. Reducing the production intensity
to neutralize footprint might cause rural societal disturbances
and intangible economic losses in the region. In such a case, at
least eco-subsidies should be offered to the farmers for their
environmental contribution. Carp production exclusively based
on natural productivity has its own limitations; high value pro-
tein from natural prey is utilized for energy supply, rather than
building biomass. Here the role of cereals, as rich source of en-
ergy, must be recognized. For producers, over-relying on cereals
for growth under low natural food availability is most likely futile
eonly aggravates environmental footprint. Yet, opportunities
exist to calibrate the present feeding practices for achieving both
environmental (minimized footprint) and aquaculture goals
(uncompromised production).
Declaration of competing interest
The authors declare that they have no known competing
nancial interests or personal relationships that could have
appeared to inuence the work reported in this paper.
CRediT authorship contribution statement
Koushik Roy: Conceptualization, Methodology, Investigation,
Formal analysis, Data curation, Writing - original draft, Visualiza-
tion. Jaroslav Vrba: Validation, Writing - review &editing, Funding
acquisition, Project administration. Sadasivam J. Kaushik: Valida-
tion, Writing - review &editing. Jan Mraz: Methodology, Valida-
tion, Resources, Writing - review &editing, Supervision, Project
administration, Funding acquisition.
Acknowledgment
The study was nancially supported by the by the Czech Science
Foundation (GACR) project No. 17-09310S. Funds from the Ministry
of Education, Youth and Sports of the Czech Republic - project
CENAKVA (LM2018099) and Biodiversity (CZ.02.1.01/0.0/0.0/
16_025/0007370) are also gratefully acknowledged. Technical
assistance of the laboratory members Dr. Petr Dvorak and Mr. Mario
Precanica during the digestibility trials are gratefully acknowl-
edged. Authors gratefully acknowledge the help of anonymous re-
viewers for improving this article.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 13
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jclepro.2020.122268.
References
Ad
amek, Z., G
al, D., Pilarczyk, M., 2009. Carp farming as a traditional type of pond
aquaculture in Central Europe: prospects and weakneses in the Czech Republic,
Hungary and Poland. Er. Aquacul. Soc. Special Pub. 37, 80e81.
Ad
amek, Z., Linhart, O., Kratochvíl, M., Flaj
shans, M., Rand
ak, T., Policar, T., Koz
ak, P.,
2012. Aquaculture in the Czech Republic in 2012: a prosperous and modern
European sector based on a thousand-year history of pond culture. World
Aquacult. 43, 20.
Aubin, J., Papatryphon, E., van der Werf, H.M.G., Chatzifotis, S., 2009. Assessment of
the environmental impact of carnivorous nsh production systems using life
cycle assessment. J. Clean. Prod. 17, 354e361. https://doi.org/10.1016/
j.jclepro.2008.08.008.
Aubin, J., Giri, S.S., Boissy, J., Mohanty, S.N., Kaushik, S.J., 2011. Environmental
Assessment Using LCA, of Fish Meal Substitution in Articial Diets of Indian
Major Carp Polyculture. Asian Pacic Aquaculture 2011. Book of abstracts, Kochi,
India, p. 246, 17-20 jan 2011.
Bashar, R., Gungor, K., Karthikeyan, K.G., Barak, P., 2018. Cost effectiveness of
phosphorus removal processes in municipal wastewater treatment. Chemo-
sphere 197, 280e290. https://doi.org/10.1016/j.chemosphere.2017.12.169.
Beke, E., Varadi, L., 2007. Multifunctional pond sh farms in Hungary. Aquacult.
Int. 15, 227e233. https://doi.org/10.1007/s10499-007-9090-5.
Bezmaternykh, V.V., Shcherbina, G.K., 2015. Sizeeweight characteristics of the late
instar larvae of chironomids (Diptera, Chironomidae) in Lake Vishtynetskoye.
Inl. Water Biol. 8, 319e324. https://doi.org/10.1134/S1995082915030037.
Biermann, G., Geist, J., 2019. Life cycle assessment of common carp (Cyprinus carpio
L.) ea comparison of the environmental impacts of conventional and organic
carp aquaculture in Germany. Aquaculture 501, 404e415. https://doi.org/
10.1016/j.aquaculture.2018.10.019.
Bogut, I., Has-Sch
on, E., Ad
amek, Z., Rajkovi
c, V., Galovi
c, D., 2007. Chironomus
plumosus larvae-a suitable nutrient for freshwater farmed sh. Poljoprivreda 13,
159 e162.
Buckwell, A., Nadeu, E., 2016. Nutrient Recovery and Reuse (NRR) in European
Agriculture. A Review of the Issues, Opportunities, and Actions. RISE Founda-
tion, Brussels. http://www.risefoundation.eu/images/les/2016/2016_RISE_
NRR_Full_EN.pdf.
Cho, C.Y., Slinger, S.J., 1979. Apparent digestibility measurement in feedstuff for
rainbow trout. In: Halver, J.E., Tiews, K. (Eds.), Finsh Nutrition and Fishfood
Technology, vol. 2. Heenemann GmbH, Berlin, pp. 239e247.
Chumchal, M.M., Drenner, R.W., 2004. Interrelationships between phosphorus
loading and common carp in the regulation of phytoplankton biomass. Arch.
Hydrobiol. 161, 147e158. https://doi.org/10.1127/0003-9136/2004/0161-0147.
Csath
o, P., Sis
ak, I., Radimszky, L., Lushaj, S., Spiegel, H., Nikolova, M.T., Nikolov, N.,
Cerm
ak, P., Klir, J., Astover, A., Karklins, A., Lazauskas, S., Kopi
nski, J., Hera, C.,
Dumitru, E., Manojlovic, M., Bogdanovi
c, D., Torma, S., Lesko
sek, M.,
Khristenko, A., 2007. Agriculture as a source of phosphorus causing eutrophi-
cation in Central and Eastern Europe. Soil Use Manag. 23, 36e56. https://
doi.org/10.1111/j.1475-2743.2007.00109.x.
Cz-Ryby, 2019. Ryb
a
rsk
e sdru
zení cesk
e republiky. http://www.cz-ryby.cz/
produkce-ryb/produkce-a-trh-ryb accessed on: 27
th
April 2019.
Duan, C., Deng, C., Gharaei, A., Wu, J., Wang, B., 2018. Selective maintenance
scheduling under stochastic maintenance quality with multiple maintenance
actions. Int. J. Prod. Res. 56, 7160e7178. https://doi.org/10.1080/
00207543.2018.1436789.
Duras, J., 2019. Chcete
cistou vodu v rybnících? Pak nepom
u
ze vyhnat ryb
a
re a
p
restat chovat kapry,
rík
a. Rozhovory, Ekolist.cz. Available online. https://
ekolist.cz/cz/publicistika/rozhovory/chcete-cistou-vodu-v-rybnicich-pak-
nepomuze-vyhnat-rybare-a-prestat-chovat-kapry-rika-jindrich-duras.
Accessed on: 5th August 2019.
Duras, J., Dziaman, R., 2010. Recovery of shallow recreational bolevecký pond, plze
n,
Czech republic. In: Nedzarek, A., Kubiak, J., T
orz, A. (Eds.), Anthropogenic and
Natural Transformation of Lakes, pp. 43e50.
Duras, J., Potu
z
ak, J., 2016. Rybníky: jakost vody a legislative. Analýzy a koment
a
re.
F
orum ochrany p
rírody 03/2016, 47-50. Available online at: http://www.casopis.
forumochranyprirody.cz/magazin/analyzy-komentare/rybniky-jakost-vody-a-
legislativa. Accessed on: 20
th
March 2019.
Duras, J., Potu
z
ak, J., 2019. Kvalita vody v rybnících a legislativa eneradostn
e
vypr
av
ení. Ekolist.cz. Available at: https://ekolist.cz/cz/publicistika/nazory-a-
komentare/duras-potuzak-kvalita-vody-v-rybnicich-a-legislativa-neradostne-
vypraveni. Accessed on: 9th September 2019.
Duras, J., Potu
z
ak, J., Kr
opfelov
a, L., Sulcova, J., Benedova, Z., Baxa, M., 2018. Hor-
usický rybník a jeho l
atkov
a balance. Rybniky 15e24. http://www.cski-cr.cz/
wp-content/uploads/2018/07/Rybniky_2018_sbornik_n.pdf.
Eumofa, 2016. Case study eprice structure in the supply chain for fresh carp in
Central Europe. European market observatory for sheries and aquaculture
products 26. https://doi.org/10.2771/961880.
Eurostat sh_aq2a, 2017. Production from aquaculture excluding hatcheries and
nurseries (from 2008 onwards) [sh_aq2a]. Available online. https://ec.europa.
eu/eurostat/web/sheries/data/database. Accessed on: 6th May 2019.
Fr
elichov
a, J., Va
ck
a
r, D., P
artl, A., Lou
ckov
a, B., Harm
a
ckov
a, Z.V., Lorencov
a, E.,
2014. Integrated assessment of ecosystem services in the Czech Republic.
Ecosyst. Serv. 8, 110e117. https://doi.org/10.1016/j.ecoser.2014.03.0 01.
Füllner, G., 2015. Traditional Feeding of Common Carp and Strategies of Replace-
ment of Fish Meal. Biology and Ecology of Carp. Taylor &Francis, Boca Raton,
pp. p135ep163.
G
al, D., Kerepeczki,
E., Gyalog, G., Pekar, F., 2015. Changimg face of central European
aquaculture: sustainability issues. Surv. Fish. Sci. 2, 42e56.
G
al, D., Pek
ar, F., Kerepeczki,
E., 2016. A survey on the environmental impact of pond
aquaculture in Hungary. Aquacult. Int. 24, 1543e1554. https://doi.org/10.1007/
s10499-016-0034-9.
Gerber, P., Uwizeye, A., Schulte, R., Opio, C., de Boer, I., 2014. Nutrient use efciency:
a valuable approach to benchmark the sustainability of nutrient use in global
livestock production? Curr. Opin. Environ. Sustain. 9 (10), 122e130. https://
doi.org/10.1016/j.cosust.2014.09.007.
Gharaei, A., Hoseini Shekarabi, S.A., Karimi, M., 2019a. Modelling and optimal lot-
sizing of the replenishments in constrained, multi-product and bi-objective
EPQ models with defective products: generalised Cross Decomposition. Int. J.
Syst. Sci. Oper. Logist. 1e13. https://doi.org/10.1080/23302674.2019.1574364.
Gharaei, A., Karimi, M., Hoseini Shekarabi, S.A., 2019b. An integrated multi-product,
multi-buyer supply chain under penalty, green, and quality control polices and
a vendor managed inventory with consignment stock agreement: the outer
approximation with equality relaxation and augmented penalty algorithm.
Appl. Math. Model. 69, 223e254. https://doi.org/10.1016/j.apm.2018.11.035.
Gharaei, A., Karimi, M., Hoseini Shekarabi, S.A., 2019c. Joint economic lot-sizing in
multi-product multi-level integrated supply chains: generalized benders
decomposition. Int. J. Syst. Sci. Oper. Logist. 1e17. https://doi.org/10.1080/
23302674.2019.1585595.
Gharaei, A., Hoseini Shekarabi, S.A., Karimi, M., Pourjavad, E., Amjadian, A., 2019d.
An integrated stochastic EPQ model under quality and green policies: gener-
alised cross decomposition under the separability approach. Int. J. Syst. Sci.
Oper. Logist. 1e13. https://doi.org/10.1080/23302674.2019.1656296.
Glencross, B.D., Booth, M., Allan, G.L., 2007. A feed is only as good as its ingredients?
a review of ingredient evaluation strategies for aquaculture feeds. Aquacult.
Nutr. 13, 17e34. https://doi.org/10.1111/j.1365-2095.2007.00450.x.
Globesh, F.A.O., 2018. European price report ejanuary 2018. Issue 1/2018, 22p.
Available online. http://www.fao.org/3/i8465en/I8465EN.pdf.
Guillen, J., Asche, F., Carvalho, N., Fern
andez Polanco, J.M., Llorente, I., Nielsen, R.,
Nielsen, M., Villasante, S., 2019. Aquaculture subsidies in the European Union:
evolution, impact and future potential for growth. Mar. Pol. 104, 19e28. https://
doi.org/10.1016/j.marpol.2019.02.045.
Hartman, P., Schmidt, G., Pietsch, C., 2015. In: Pietsch, C., Hirsch, P. (Eds.), Carp
Aquaculture in Europe and Asia, pp. 77e80.
Hejzlar, J.,
S
amalov
a, K., Boers, P., Kronvang, B., 2006. Modelling phosphorus
retention in lakes and reservoirs. In: The Interactions between Sediments and
Water. Springer Netherlands, Dordrecht, pp. 123e130. https://doi.org/10.1007/
978-1-4020-5478-5_13.
Henriksson, P.J.G., Heijungs, R., Dao, H.M., Phan, L.T., de Snoo, G.R., Guin
ee, J.B., 2015.
Product carbon footprints and their uncertainties in comparative decision
contexts. PloS One 10, e0121221. https://doi.org/10.1371/journal.pone.0121221.
Hoseini Shekarabi, S.A., Gharaei, A., Karimi, M., 2019. Modelling and optimal lot-
sizing of integrated multi-level multi-wholesaler supply chains under the
shortage and limited warehouse space: generalised outer approximation. Int. J.
Syst. Sci. Oper. Logist. 6, 237e257. https://doi.org/10.1080/
23302674.2018.1435835.
Hua, K., Bureau, D.P., 2010. Quantication of differences in digestibility of phos-
phorus among cyprinids, cichlids, and salmonids through a mathematical
modelling approach. Aquaculture 308, 152e158. https://doi.org/10.1016/
j.aquaculture.2010.07.040.
Huang, H., Xiao, D., Liu, J., Hou, L., Ding, L., 2015. Recovery and removal of nutrients
from swine wastewater by using a novel integrated reactor for struvite
decomposition and recycling. Sci. Rep. 5, 10183. https://doi.org/10.1038/
srep10183.
Icar (Indian Council of Agricultural Research), 2011. Handbook of Fisheries and
Aquaculture. Indian Council of Agricultural Research, New Delhi, India.
Jahan, P., Watanabe, T., Satoh, S., Kiron, V., 2002. A laboratory-based assessment of
phosphorus and nitrogen loading from currently available commercial carp
feeds. Fish. Sci. 68, 579e586. https://doi.org/10.1046/j.1444-2906.2002.0 0464.x.
Jahan, P., Watanabe, T., Kiron, V., Satoh, S., 2003. Balancing protein ingredients in
carp feeds to limit dischargeof phosphorus and nitrogen into water bodies. Fish.
Sci. 69, 226e233. https://doi.org/10.1046/j.1444-2906.2003.0 0612.x.
Kainz, E., 1985. Zur Auswirkung von Karpfenteichabüssen auf die Wasserqualit
at
von Vorutem.
Oster Fisch 38, 88e96.
Kaushik, S.J., 1980. Inuence of nutritional status on the daily patterns of nitrogen
excretion in the carp (Cyprinus carpio L.) and the rainbow trout (Salmo
gairdneri R.). Reprod. Nutr. Dev. 20, 1751e1765. https://doi.org/10.1051/rnd:
19801002.
Kaushik, S.J., 1995. Nutrient requirements, supply and utilization in the context of
carp culture. Aquaculture 129, 225e241. https://doi.org/10.1016/0044-8486(94)
00274-R.
Kn
osche, R., Schreckenbach, K., Pfeifer, M., Weissenbach, H., 2000. Balances of
phosphorus and nitrogen in carp ponds. Fish. Manag. Ecol. 7, 15e22. https://
doi.org/10.1046/j.1365-2400.2000.00198.x.
Kopp, R.,
Rezní
ckov
a, P., Hada
sov
a, L., Petrek, R., Brabec, T., 2016. Water quality and
K. Roy et al. / Journal of Cleaner Production 270 (2020) 12226814
phytoplankton communities in newly created shponds. Acta Univ. Agric. Silvic.
Mendelianae Brunensis 64, 71e80. https://doi.org/10.11118/
actaun201664010071.
Kronvang, B., Vagstad, N., Behrendt, H., Bøgestrand, J., Larsen, S.E., 2007. Phosphorus
losses at the catchment scale within Europe: an overview. Soil Use Manag. 23,
104e116 . https://doi.org/10.1111/j.1475-2743.20 07.0 0113.x.
Kufel, L., 2012. Are shponds really a trap for nutrients? ea critical comment on
some papers presenting such a view/Czy stawy rybne sa˛rzeczywi
scie pułapka˛
dla pierwiastk
ow biogennych? ekrytyczny komentarz do pewnych prac pre-
zentuja˛cych taki pogla˛d. J. Water Land Dev. 17, 39e44. https://doi.org/10.2478/
v10025-012-0031-y.
Lamarra, V.A., 1975. Digestive activities of carp as a major contributor to the
nutrient loading of lakes. SIL Proceedings 2461e2468. https://doi.org/10.1080/
03680770.1974.11896330, 1922-2010 19.
Leip, A., Achermann, B., Billen, G., Bleeker, A., Bouwman, A.F., de Vries, W.,
Dragosits, U., D
oring, U., Fernall, D., Geupel, M., Herolstab, J., Johnes, P., Le
Gall, A.C., Monni, S., Neve
ce
ral, R., Orlandini, L., Prudhomme, M., Reuter, H.I.,
Simpson, D., Seufert, G., Spranger, T., Sutton, M.A., van Aardenne, J., Voß, M.,
Winiwarter, W., 2011. Integrating nitrogen uxes at the European scale. In:
Sutton, M.A., Howard, C.M., Erisman, J.W., Billen, G., Bleeker, A., Grennfelt, P.,
van Grinsven, H., Grizzetti, B. (Eds.), The European Nitrogen Assessment.
Cambridge University Press, Cambridge, pp. 345e376. https://doi.org/10.1017/
CBO9780511976988.019.
Leip, A., Weiss, F., Lesschen, J.P., Westhoek, H., 2014. The nitrogen footprint of food
products in the European Union. J. Agric. Sci. 152, 20e33. https://doi.org/
10.1017/S0021859613000786.
Leip, A., Billen, G., Garnier, J., Grizzetti, B., Lassaletta, L., Reis, S., Simpson, D.,
Sutton, M.A., de Vries, W., Weiss, F., Westhoek, H., 2015. Impacts of European
livestock production: nitrogen, sulphur, phosphorus and greenhouse gas
emissions, land-use, water eutrophication and biodiversity. Environ. Res. Lett.
10, 115004. https://doi.org/10.1088/1748-9326/10/11/115004.
Mackay, E.B., Maberly, S.C., Pan, G., Reitzel, K., Bruere, A., Corker, N., et al., 2014.
Geoengineering in lakes: welcome attraction or fatal distraction? Inland Waters
4 (4), 349e356.
MacLeod, M., Hasan, M.R., Robb, D.H.F., Mamun-Ur-Rashid, M., 2019. Quantifying
and Mitigating Greenhouse Gas Emissions from Global aquaculture. FAO Fish-
eries and Aquaculture Technical Paper No. 626. FAO, Rome.
Mangi, H.O., 2016. Estimation of monetary values of the ecosystem services ow at
the tidal elbe river. Adv. Ecol. 2016, 1e8. https://doi.org/10.1155/2016/6742786.
Mazurkiewicz, J., 2009. Utilization of domestic plant components in diets for
common carp Cyprinus carpio L. Arch. Pol. Fish. 17 https://doi.org/10.2478/
v10086-009-0001-4.
Molinos-Senante, M., Hern
andez-Sancho, F., Sala-Garrido, R., Garrido-Baserba, M.,
2011. Economic feasibility study for phosphorus recovery processes. Ambio 40,
408e416. https://doi.org/10.1007/s13280-010-0101-9.
Mungkung, R., Aubin, J., Prihadi, T.H., Slembrouck, J., van der Werf, H.M.G.,
Legendre, M., 2013. Life Cycle Assessment for environmentally sustainable
aquaculture management: a case study of combined aquaculture systems for
carp and tilapia. J. Clean. Prod. 57, 249e256. https://doi.org/10.1016/
j.jclepro.2013.05.029.
Musil, M., Novotn
a, K., Potu
z
ak, J., H
uda, J., Pechar, L., 2014. Impact of topmouth
gudgeon (Pseudorasbora parva) on production of common carp (Cyprinus
carpio) dquestion of natural food structure. Biologia 69. https://doi.org/
10.2478/s11756-014-0483-4.
Nrc, National Research Council, 2011. Nutrient Requirements of Fish and Shrimp.
National Academies Press, Washington, D.C. https://doi.org/10.17226/13039.
Nwanna, L.C., Lemme, A., Metwally, A., Schwarz, F.J., 2012. Response of common
carp (Cyprinus carpio L.) to supplemental DL-methionine and different feeding
strategies. Aquaculture 356e357, 365e370 . https://doi.org/10.1016/
j.aquaculture.2012.04.044.
Ol
ah, J., Szab
o, P., Esteky, A.A., Nezami, S.A., 1994. Nitrogen processing and retention
in Hungarian carp farms. J. Appl. Ichthyol. 10, 335e340. https://doi.org/10.1111/
j.1439-0426.1994.tb00174.x.
OHagan, A.M., Corner, R.A., Aguilar-Manjarrez, J., Gault, J., Ferreira, R.G.,
Ferreira, J.G., OHiggins, T., Soto, D., Massa, F., Bacher, K., Chapela, R., Fezzardi, D.,
2017. Regional Review of Policy-Management Issues in Marine and Freshwater
Aquaculture. Report Produced as Part of the Horizon 2020 AquaSpace Project,
p. 170.
Papatryphon, E., Petit, J., Werf, H.M.G.v.d., Kaushik, S.J., 2004. Life Cycle Assessment
of trout farming in France: a farm level approach. DIAS Rep. Animal Hus. 71e77.
Pechar, L., 2000. Impacts of long-term changes in shery management on the
trophic level water quality in Czech sh ponds. Fish. Manag. Ecol. 7, 23e31.
https://doi.org/10.1046/j.1365-2400.2000.0 0193.x.
Philis, G., Ziegler, F., Gansel, L.C., Jansen, M.D., Gracey, E.O., Stene, A., 2019.
Comparing life cycle assessment (LCA) of salmonid aquaculture production
systems: status and perspectives. Sustainability 11, 2517. https://doi.org/
10.3390/su11092517.
Pokorný, J., Hauser, V., 2002. The restoration of sh ponds in agricultural land-
scapes. Ecol. Eng. 18, 555e574. https://doi.org/10.1016/S0925-8574(02)00020-4.
Popp, J., B
eke, E., Duleba, S., Ol
ah, J., 2019. Multifunctionality of pond sh farms in
the opinion of the farm managers: the case of Hungary. Rev. Aquacult. 11,
830e847. https://doi.org/10.1111/raq.12260.
Potu
z
ak, J., Duras, J., Drozd, B., 2016. Mass balance of shponds: are they sources or
sinks of phosphorus? Aquacult. Int. 24, 1725e1745. https://doi.org/10.1007/
s10499-016-0071-4.
Prchal, M., Bugeon, J., Vandeputte, M., Kause, A., Vergnet, A., Zhao, J., Gela, D.,
Genestout, L., Bestin, A., Haffray, P., Kocour, M., 2018. Potential for genetic
improvement of the main slaughter yields in common carp with in vivo
morphological predictors. Front. Genet. 9 https://doi.org/10.3389/
fgene.2018.00283.
Prikryl, I., 1983. Effects of sh culture intensication on water quality in sh ponds.
Bull. Vurh Vodn. 19, 3e16.
R Development Core Team, 2015. R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna, Austria. URL.
https://www.R-project.org/.
Ramseyer, L.J., 2002. Predicting whole-sh nitrogen content from sh wet weight
using regression analysis. N. Am. J. Aquacult. 64, 195e204. https://doi.org/
10.1577/1548-8454(2002)064<0195:PWFNCF>2.0.CO;2.
Rerat, A., Kaushik, S.J., 1995. Nutrition, animal production and the environment.
Water Sci. Technol. 31 https://doi.org/10.1016/0273-1223(95)00422-J.
Richards, I.R., Dawson, C.J., 2008. Phosphorus imports, exports, uxes and sinks in
Europe. In: Proceedings 638, International Fertilizer Society, York (UK),
pp. 1e28.
Rosendorf, P., Vysko
c, P., Prchalov
a, H., Fiala, D., 2016. Estimated contribution of
selected non-point pollution sources to the phosphorus and nitrogen loads in
water bodies of the Vltava river basin. Soil Water Res. 11, 196e204. https://
doi.org/10.17221/15/2015-SWR.
Roy, K., Vrba, J., Kaushik, S.J., Mraz, J., 2019. Feed-based common carp farming and
eutrophication: is there a reason for concern? Rev. Aquac. raq. 12407 https://
doi.org/10.1111/raq.12407.
Schwarz, F.J., Kirchgessner, M., Deuringer, U., 1998. Studies on the methionine
requirement of carp (Cyprinus carpio L.). Aquaculture 161, 121e129. https://
doi.org/10.1016/S0044-8486(97)00262-7.
Sim
ci
c, T., Brancelj, A., 1997. Electron transport system (ETS) activity and respiration
rate in ve Daphnia species at different temperatures. In: Cladocera: the
Biology of Model Organisms. Springer Netherlands, Dordrecht, pp. 117e125.
https://doi.org/10.1007/978-94-011-4964-8_13.
Steffens, W., 1986. Intensive Fish Production. PWRiL, Warszawa, pp. 11e417 (in
Polish).
Sterni
sa, M., Mraz, J., Mo
zina, S.J., 2017. Common carp - still unused potential. Meso
19, 434e439.
Szücs, I., Stündl, L., V
aradi, L., 2007. Carp farming in central and eastern Europe and
A case study in multifunctional aquaculture. In: Species and System Selection
for Sustainable Aquaculture. Blackwell Publishing, Ames, Iowa, USA,
pp. 389e414. https://doi.org/10.1002/9780470277867.ch26.
van Dijk, K.C., Lesschen, J.P., Oenema, O., 2016. Phosphorus flows and balances of the
European union member states. Sci. Total Environ. 542, 1078e1093. https://
doi.org/10.1016/j.scitotenv.2015.08.048.
Velthof, G.L., Oudendag, D.A., Oenema, O., 2007. Development and Application of
the Integrated Nitrogen Model MITERRA-EUROPE, vol. 102. Alterra, Wagenin-
gen. Alterra Report.
Vinten, A.J.A., Martin-Ortega, J., Glenk, K., Booth, P., Balana, B.B., MacLeod, M.,
Lago, M., Moran, D., Jones, M., 2012. Application of the WFD cost proportionality
principle to diffuse pollution mitigation: a case study for Scottish Lochs.
J. Environ. Manag. 97, 28e37. https://doi.org/10.1016/j.jenvman.2011.10.015.
V
seti
ckov
a, L., Ad
amek, Z., Rozko
sný, M., Sedl
a
cek, P., 2012. Effects of semi-intensive
carp pond farming on discharged water quality. Acta Ichthyol. Piscatoria 42,
223e231. https://doi.org/10.3750/AIP2011.42.3.06.
Vystavna, Y., Hejzlar, J., Kop
a
cek, J., 2017. Long-term trends of phosphorus con-
centrations in an articial lake: socio-economic and climate drivers. PloS One
12, e0186917. https://doi.org/10.1371/journal.pone.0186917.
Watanabe, T., Jahan, P., Satoh, S., Kiron, V., 1999. Total phosphorus loading onto the
water environment from common carp fed commercial diets. Fish. Sci. 65,
712e716. https://doi.org/10.2331/shsci.65.712.
Weiss, F., Leip, A., 2012. Greenhouse gas emissions from the EU livestock sector: a
life cycle assessment carried out with the CAPRI model. Agric. Ecosyst. Environ.
149, 124e134. https://doi.org/10.1016/j.agee.2011.12.015.
Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag,
New York. https://doi.org/10.1007/978-3-319-24277-4.
Woynarovich, A., Moth-Poulsen, T., P
eteri, A., 2010. Carp Polyculture in Central and
Eastern Europe, the Caucasus and Central Asia: a Manual, vol. 554. Food and
Agriculture Organization of the United Nations.
Woynarovich, A., Bueno, P.B., Altan, O., Jeney, Z., Reantaso, M., Xinhua, Y., Van
Anrooy, R., 2011. Better Management Practices for Carp Production in Central
and Eastern Europe, the Caucasus and Central Asia. FAO, Rome. FAO Fisheries
and Aquaculture Technical Paper 566.
Zemanov
a, J.,
Sorf, M., Hejzlar, J.,
Sorfov
a, V., Vrba, J., 2019. Planktivorous sh
positively select Daphnia bearing advanced embryos. Mar. Freshw. Res. 71,
505e511. https://doi.org/10.1071/MF18466.
Rezní
ckov
a, P., Petrovajov
a, V., Nerudov
a, J., Hada
sov
a, L., Kopp, R., 2016. The colo-
nization of newly built shponds by the macroinvertebrate assemblages. Acta
Univ. Agric. Silvic. Mendelianae Brunensis 64, 141e149. https://doi.org/10.11118/
actaun201664010141.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 15
... Besides, carp farming and fishponds together provide tangible production services (gross farm-gate income € ha − 1 ). It is also one of the cleanest food production, with N, P footprint 1.5-4 times less than that of EU crop-livestock averages (Roy et al., 2020b). In the CEER, presently fish contribute ~15% of total animal sourced protein on consumers plate including fish, meat, and eggs (Miller et al., 2022). ...
... Besides, market prices of whole, live common carp sold at farm-gate have not increased significantly in most European countries. Present farm-gate prices of carp in some CEER countries are stagnant in the range of ~2-2.5 € kg − 1 live weight (Roy et al., 2020b). ...
... It is mainly due to synergistic top-down and bottom-up effects of fish stock and nutrient legacy, respectively (Roy et al., 2020a). Fishponds are also among the most biodiverse and ecologically critical freshwater habitats (Frélichová et al., 2014;Hill et al., 2018;Roy et al., 2020b). Concerns exist on the effect of semi-intensive carp farming (feeding) in present-day fishponds on additional nutrients enrichment, eutrophication, ecosystem functioning and biodiversity. ...
Article
Full-text available
The present work aimed to understand nutrient enrichment and resultant eutrophication caused by carp farming in semi-intensively managed, temperate shallow-lake ecosystems like central European fishponds – combining animal nutrition and plankton ecology group model principles. In the traditional yet predominant pond farming in central Europe, carp stocks start the vegetative season on a ketogenic diet (high in natural food), have a balanced diet shortly in mid-season (cereals introduced as supplementary feed), and end on a starchy diet (high in cereals). Under beginning-season diets, the fish (carp) stock exhibit high but non-bioeconomic N and P retentions. With a surplus of ‘digestible’ N (protein, amino acids) relative to insufficient carbohydrate energy, much of the digested N is pumped back to the environment in algae-reactive forms (NH4–N). A surplus of digestible P per unit of digestible N also triggers renal clearance of digested P; pumped back to environment as PO4³⁻. By the end-of-season, N, P retentions deteriorate significantly due to high metabolic N losses caused by missing digestible amino acids (lysine, isoleucine) and decreased P digestibility, respectively. Little digested P is unutilized and even discarded in tandem with poor N deposition. End-of-season feeding in fishponds is perhaps most polluting and triggers de-novo lipogenesis, instead of protein (biomass) accretion. However, the ratio of reactive losses (to suspended losses) of N, P, which could instantly trigger algal assimilation, is equally high (bad) at the beginning- and end-of-season. We show aggravated N, P loading by carp may occur both under high and low zooplankton-zoobenthos availability, contradictory to prevailing notions. Environmental nutrient loading by carps is most suppressed, including lowest reactive N, P losses, when diet is balanced. Carp farming in regional fishponds could benefit by adopting scientifically sound ‘pond feeds’ and managing carps' satiety to graze (or spare) zooplankton-zoobenthos for prolonging clear-water phase.
... We recognize that perhaps nutrition (and resultant excretion) is the most dynamic and regular process in living organisms, which involves the exchange of nutrients to and/or from the environment [6,[14][15][16][17][18][19][20]. In an aquaponic system, fish feed is intended to be the only daily nutrient input, followed by pH adjustment buffers or carbon sources, not artificial fertilizers. ...
... Fish feed is hereinafter referred to as aquafeed. Fishes through their particulate fecal (digestible) and dissolved non-fecal (metabolic) excretion may be regarded as pumps of nutrients for plants [19,20] via microbial digesters [6,21]. Feeding and excretion processes may be increasingly targeted for bio-manipulation to address improved nutrient loop or circularity from animal (in vivo) to farm (in situ) level. ...
... Apart from the digestible losses (= 100 − ADC% of crude intake) from fish, the metabolizable losses (= 100 − retention% − digestible losses% of crude intake) also contribute significant environmental loading of nutrients from the fish [14,16,[18][19][20]24]. The digestible losses, also termed fecal losses, are particulate matter, which need microbes to mineralize the nutrients into reactive forms that the plants can readily assimilate. ...
Article
Full-text available
Future food systems aim to achieve improved resource use efficiency and minimized environmental footprint through a circular bioeconomy-based approach. Aquaponics is a hallmark of such circular food production. The image of a circular nutrient utilization efficiency in aquaponics is often weakened by the daily use of additional inorganic fertilizers in such systems. As circular bioeconomy greatly emphasizes developing bio-based solutions, the presented novel inventory ‘TilaFeed’ and its associated utility tools is a step towards achieving more circular nutrient utilization and bioeconomy in future aquaponics. Through the formulation of tailored fish feed that is compatible with aquaponic systems’ needs (e.g. plant nutrient requirement, mineralization efficiency of microbial sludge digesters), the objectives of TilaFeed are (i) to solve nutrient constraints in aquaponic systems, both for fish and plants; (ii) to avoid or strongly limit artificial fertilizer use in aquaponics by smartly tailored aquafeeds; and (iii) to equip system managers with decision-making tools for improved nutrient planning of their aquaponic systems. TilaFeed is a bio-based inventory. It integrates material (nutrient) flow information from feed to fish (in-vivo nutrient partitioning, forms of excretion) to environment (in-situ nutrient loading, nutrient forms) and primary producers (mineralization by microbes, available nutrients to plants). Based on TilaFeed-Model, feed for future aquaponics may be more precisely formulated with the principle that nutrients are not only a resource for fish, but excreted nutrients from fish (feed) also fertilize the microbes and plants.