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Nutrient footprint and ecosystem services of carp production in
European fishponds 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 efficiency
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 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 enutrient footprint (~9.4e10.8 kg N ha
1
, ~2.7e3.2 kg P
ha
1
;1.5e4<EU crop-livestock sectors); nutrient utilization efficiencies (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 identified, 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 fishponds 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 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 (uncompro-
mised production) are discussed.
©2020 Elsevier Ltd. All rights reserved.
1. Introduction
For decades, the ‘land-locked’central European countries have
been relying mostly on carp culture for fisheries production
(Ad
amek et al., 2012;G
al et al., 2015;Woynarovich et al., 2011).
Common carp (Cyprinus carpio L.) farming in fishponds 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 fishponds (Eurostat
fish_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 fish_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 intensification 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 fishponds 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 fishponds, ~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
ratified environmental legislations in place (reviewed in O’Hagan
et al., 2017).
Unlike Asian fishponds, fertilizing fishponds 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 flush it out (Kn€
osche et al., 2000;
Potu
z
ak et al., 2016), while some perform green manuring on dried
pond beds and later filling them (Hartman et al., 2015). This nar-
rows it down to a more regular practice i.e. supplementary feeding;
probably the only major, ‘deliberate’allochthonous nutrient source.
The leading role played by feed and feeding efficiency 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 artificial 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 fishponds
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 fishpond-
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 substance’applied to fishponds (Duras and Potu
z
ak,
2019). Such stringent measures or presumptions restricting the
intensity of carp farming in European fishponds, in order to reduce
environmental footprint, have impacts on commercial viability too.
The market prices of common carp have in fact come down
significantly in most European countries (FAO Globefish, 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;
O’Hagan et al., 2017) or even lower (1.9 Vkg
1
live weight) in
Hungary (FAO Globefish, 2018). Although the concerns of envi-
ronmentalists are in good faith, however, being too harsh on carp
farming without ‘clarified’knowledge is unfair.
In order that sustainable management strategies in aquaculture
be based on environmental impact analyses, life cycle assessment
(LCA) often is the first 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 fishponds (Biermann and Geist, 2019).
These LCAs were more focused on ‘percentage contribution’of
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 (fishponds) 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 fishponds, employing different
methodologies; (b) nutrient footprint of carp production in com-
parison to EU crop and livestock production; (c) nutrient utilization
efficiencies by carps in fishponds 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
fishponds; (f) required production intensity in fishponds 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 findings 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 fit 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 fishponds i.e. natural
food or cereals)
FCR
cereals
Relative FCR of cereals in the presence of carp’s
natural food in fishponds
FCR
natural prey
Relative FCR of carp’s natural food in the
presence of cereals as supplementary feed
CEER Central Eastern European region
EU European Union
NUE Nutrient Utilization Efficiency
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 fish-
ponds; yield 449.4 kg ha
1
) was obtained from CZ-Ryby (2019).
Relative feeding coefficient (i.e. relative food conversion ratio in the
presence of natural food) of cereals supporting carp production in
fishponds 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 carp’s
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 ‘FCR’implies food conversion ratio (¼dietary intake ∕
biomass gain) in relative sense. FCR
cereals
imply FCR of cereals in the
presence of carp’s natural food in fishponds. FCR
natural prey
imply
FCR of carp’s 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 fishponds (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
fulfill 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 fishponds (wheat, corn, triticale) and carp’s 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 coefficients 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 fishponds 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;O’Hagan et al., 2017). All these metadata were used for
further comparison or calculation (indicated below).
3. Calculation
3.1. N and P losses from carp’s feeding in fishponds
N and P losses from carp’s feeding in fishponds 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 efficiency 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 fishponds (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 coefficient.
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 fishponds or introduced to the fishponds from
outside, respectively.
3.4. Environmental cost burden and ecosystem services of carp
production in fishponds
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 fishponds in Czech Republic (1257 V
ha
1
); (b) commercial production services offered by fishponds
(~2e2.5 Vkg
1
live weight), and; (c) valuation of autochthonous
nutrient removed (cost mentioned above). All valuations were
made on ‘per ha fishpond’basis.
3.5. Neutral-footprint carp production scenario
The required cereals-based production intensity in fishponds to
neutralize existing footprint to ‘near-zero’levels was coined as
‘neutral footprint’production. For its mathematical derivation,
median values between ‘exclusively natural’and ‘existing’pro-
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 scenario’was 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 natural’to ‘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. fulfilled 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 fitting (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 benefit
(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 figures 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 fishponds (corn, triticale, wheat) is 2.62%
and 0.58%, respectively. Carp’s 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 carp’s feeding in fishponds
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 fishponds (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
fishpond. 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 fishponds (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. Carp’s 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
fishpond. 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 carp’s
feeding activity in fishponds 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 fishponds 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 fishponds 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 efficiency 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
fishpond), NUE
N
in fishponds 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
fishpond; output carp biomass: ~8.6 kg N and ~2.3 kg P ha
1
fishpond), 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 fishponds. 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 fishponds. 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 efficient 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 fishponds
The environmental cost burden, under the present production
regime, was estimated at ~72e184 Vha
1
. Whereas, ecosystem
services offered by carp production and fishponds 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
worth’of 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 fishponds, 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
fishpond and 0.2 (negligible) to 0.5 kg P
ha
1
fishpond. Although theoretically proposed, some application
bottlenecks might render its practicality questionable (clarified
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 fishponds (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
fishpond
28.7e38.3 kg N ton carp
1
12.9e17.2 kg N ha
1
fishpond
11.6e14.5 kg P ton carp
1
5.2e6.5 kg P ha
1
fishpond
3.6e4.8 kg P ton carp
1
1.6e2.1 kg P ha
1
fishpond
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
fishpond
9.9e18.2 kg N ton carp produced
1
4.5e8.2 kg N ha
1
fishpond
8.7e11.6 kg P ton carp
1
3.9e5.2 kg P ha
1
fishpond
0.7e0.9 kg P ton carp produced
1
0.3e0.4 kg P ha
1
fishpond
N:P ~3:1e4:1 N:P ~14:1e20:1
Spatial footprint on environment (per ha fishpond)
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 fulfilling combinations of relative FCRs have been
identified as ‘green zones’in Ta ble 3 . To reduce the use of cereals
(by 15% to 25%) in fishponds, 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
(modified scenario; Table 3). Although this 25% (þ0.1 FCR) in-
crease of dependency on natural prey appears theoretically
promising, it is difficult practically (discussed below). Multiple
linear models for calibrating digestible nutrient supply in fish-
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 fishponds, 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 fishpond ecosystem.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 1222686
inevitable consequences on magnification 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 identified 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 profile is based on five 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 efficiencies 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 significantly higher figures 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 fishponds in CEER,
coupled with production value and regulatory services of fishponds
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 coefficient) combinations for optimum carp
growth in fishponds.
Fig. 3. Comparative account of ecosystem services (above red line) and environmental cost burden (below red line): Carp production in fishponds 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 figure 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 fishponds (~1257 Vha
1
) is worth ~74.5e100.6 million Von
national scale (Table 4). The positive services of carp farming in
European fishponds 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 first 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 first 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) profile. Deficiencies 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 first 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 carp’s feeding in fishponds
Within Europe, especially from the Central region, only a
handful of ‘published’estimates on carp fishpond 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 fishponds. Point of inter-section denote trade-off FCRs (cereals 2.2
and natural prey 0.35) to reduce faecal nutrient losses in fishponds (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 efficiency 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. Profile 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 fishpond 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 fishponds, 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 five common carp producing countries in Europe.
K. Roy et al. / Journal of Cleaner Production 270 (2020) 122268 9
carp produced; and, (c) fishponds have special benefits 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 fishponds 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 fluctuation of nutrients in fishponds 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 fishponds beyond carp’s excretory losses from feeding
Fig. 5. Breakdown (million V) of different eco-services associated with carp production in fishponds 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 fishponds worth ~1257 Vha
1
.
Fig. 6. Worth of positive (right of dotted line) and negative (left) ecosystem services from carp production in fishponds 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 fishponds per production cycle. Assuming 5 carp production cycles during 20 00e2014, carp
aquaculture ‘alone’might 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 inflow water or
catchment fertilization. The present work highlights this over-
looked interference in most fishpond 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 fishponds. They demonstrated ‘mass
balanced’results when validated under practical conditions seldom
make any sense. Alternative nutrient budgeting methods more
appropriate for Central European fishponds were proposed (Hejzlar
et al., 2006;Potu
z
ak et al., 2016). Our results, if compared with the
‘mass-balanced’results, 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 findings.
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 fishpond-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 fishponds (e.g. outflow water-P <inflow
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 quantified footprint might
not always end-up enriching downstream waters. Long term water-
residence period is known to precipitate P into fishpond 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 fishponds, following which, the commercial interests of ‘profit-
able’carp production may falter edespite fulfilling ‘greener-goals’.
Downscaling the existing production to ‘neutral’or ‘natural’modes
may reduce earning by at least 170 Vha
1
or 223 Vha
1
respectively. This view, from environmentalist’s perspective, is a
traditional argument ‘sold’by the producers. Present production
regime, with ‘still intact’commercial 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 fish-
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 fishponds 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 fishponds
as relatively ‘cleaner’way 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 fishponds 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 efficiency (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
fishponds, 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 fishponds; 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 fishponds. During late spring to summer,
Czech fishponds 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
fishponds. 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 fishponds 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 balanced’results (explained in
supplementary text). In terms of autochthonous nutrient extrac-
tion, present production regime is only ~1.5e2.2 times less efficient
than natural carp production. A more precise estimation would
require stable-isotopes approach; conveniently for N but difficult
for P. Nonetheless, greater retention of dietary N and P by farmed
fish 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 fishponds
Carp production in European fishponds has been ‘qualitatively’
attributed to various positive services (Szücs et al., 2007;Bekefiand
Varadi, 2007,Popp et al., 2019). Ecosystem services include flood
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 fishponds. In
addition, the production benefit(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 fish 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 fishponds 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 fishpondsismanyfoldshigher(~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 environmentalists’interests (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 fishponds 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 fish-
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 filtering equivalent numbers of active nat-
ural prey(s) in fishponds. Cereals itself are rich and easy source of
digestible energy for carps (~2759.4 kcal kg
1
; our data) having an
energy profile 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
fishpond 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 efficiency 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 fish-
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
fishpond effluents (Biermann and Geist, 2019). Here, using an
alternative approach, we highlighted the same and quantified it.
To the best of our knowledge, this is the firstdata-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 fishponds 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 fishponds), or
inadequate supply of digestible nutrients for carp’soptimum
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 profile of
carp’sdietinfishponds, 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 feed’under 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-subsidies’for their environmental
contribution. To some extent, this would offset their decreased
farm-gate income.
6. Conclusion
The present study revealed that carp production in fishponds
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 fishponds. The ecosystem and production ser-
vices offered by carp farming in fishponds have immense societal
and economic advantages. Majority of nutrient footprint from
carp’s feeding activity is contributed by supplementary feeding
with cereals. Monetary benefit 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
financial interests or personal relationships that could have
appeared to influence 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 financially 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.
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