Aquaculture Research, 2016, 47, 2917–2927
12743
Earthworm powder as an alternative protein source
in diets for common carp (Cyprinus carpio L.)
Tuan Nguyen Ngoc1,2, Johannes Pucher1, Klaus Becker1 & Ulfert Focken1,3
1
Department of Aquaculture Systems in the Tropics and Subtropics (480b), Universitaet Hohenheim, Stuttgart,
Germany
2
Faculty of Fisheries, Vietnam National University of Agriculture, Hanoi, Vietnam
3
Thuenen-Institute of Fisheries Ecology, Ahrensburg, Germany
Correspondence: U Focken, Th€
unen-Institute of Fisheries Ecology, Federal Research Institute for Rural Areas, Forestry and
Fisheries, Wulfsdorfer Weg 204, D-22926 Ahrensburg, Germany. Email: ulfert.focken@ti.bund.de
Abstract
The increasing need for aquafeed resources and
the finite availability of conventional feed
resources are making it necessary to search for
alternative high-protein resources that are not
used as human food. The earthworm Perionyx
excavatus was tested as a feed ingredient in diets
for common carp. An experiment was conducted
to evaluate the potential of earthworm powder as
a replacement for fishmeal. In a recirculation
aquarium system, triplicate groups of five common
carp (Cyprinus carpio L.) were fed a control feed
(fishmeal based protein), or experimental diets in
which 30% (EW30), 70% (EW70), or 100%
(EW100) of fishmeal protein was replaced by
earthworm protein. Fish growth, feed digestibility
and feed utilization were monitored. Growth rate,
protein efficiency and energy retention in fish
were similar (EW30, EW100) or higher (EW70)
for diets containing earthworm meal compared to
the control diet. Protein digestibility in EW30,
EW70 and EW100 was higher than in the control
diet, but in (EW100), lipid conversion was lower.
We conclude that earthworm is a suitable partial
replacement for fishmeal in feeds for common
carp.
Keywords: alternative feed ingredient,
earthworm, fishmeal replacement, common carp
Introduction
Aquaculture is one of the fastest growing sectors
in food production with annual growth rates
© 2015 John Wiley & Sons Ltd
doi:10.1111/are.
between 5.1% and 7.4% between 2007 and 2012
(SOFIA 2014). This increasing production requires
corresponding increases in aquafeed production
(Tacon & Metian 2008). As fishmeal, the tradi-
tional source of animal protein for aquafeeds, is
finite (Naylor, Hardy, Bureau, Chiu, Elliott, Farrell,
Forster, Gatlin, Goldburg, Hua & Nichols 2009),
various other protein resources have been studied
and applied in aquafeeds such as soybean meal,
various other plant proteins and rendered animal
products (Hardy 2010; Hern andez, Olvera-Novoa,
Hardy, Hermosillo, Reyes & GonzAlez  2010).
Apart from the feed resources produced on a large
scale and traded internationally, a number of
highly nutritive feed resources have been sug-
gested that can be produced on a small scale and
mainly utilized and traded locally or regionally.
These include silk worm pupae meals (Begum,
Chakraborty, Zaher, Abdul & Gupta 1994), house-
fly maggots (Ogunji, Kloas, Wirth, Neumann &
Pietsch 2008), snails and termites (Phonekhamph-
eng, Hung & Lindberg 2008) and various earth-
worm species (e.g. Tacon, Stafford & Edwards
1983; Nandeesha, Srikanth, Basavaraja, Keshav-
anath, Varghese, Bano, Ray & Kale 1988; Paripu-
ranam, Divya, Ulaganathan, Balamurugan &
Umamaheswari 2011).
The production of earthworm (vermiculture)
can be performed either on a small scale (Cha-
krabarty, Das & Das 2011) or semi-industrially
(Sinha, Herat, Agarwal, Asadi & Carretero
2002). So far, the latter has been practiced
mainly as a means of organic waste management
(Suthar 2009a,b; Yadac & Garg 2009; Sim &
Wu 2010).
2917
Earthworm meal in feeds for common carp T N Ngoc et al. Aquaculture Research, 2016, 47, 2917–2927

In 1981, earthworm was realized as a potential

Materials and methods
source of protein for animal feeds (Hartenstein
1981). A number of earthworm species have since
Experimental feeds
been studied in detail for their suitability in differ-
ent fish species. Tacon et al. (1983) reported that Earthworm P. excavatus was purchased from a
different earthworm species contain about small-scale commercial vermiculture facility in
50–60% of crude protein (CP) in dry matter (DM) suburban Hanoi (Viet Nam) that produces earth-
and have low ash content which is a favourable worm on a substrate of ruminant manure for use
characteristic for an ingredient of fish feed. Tacon in feeds and traditional medicines. The worms
et al. (1983) tested the possibility of partially were cleaned from soil, frozen, freeze-dried and
substituting fishmeal by earthworm (Eisenia foet- vacuum-packed for transportation to the Univer-
ida, Allolobophora sp. and Lumbricus terrestis) in sity of Hohenheim (Germany). Fishmeal as feed
trout diets and reported the latter two species as ingredient was purchased from a large feed retailer
well suited for the substitution of fishmeal in diets in Germany (Vereinigte Fischmehlwerke Cuxha-
for rainbow trout, for the first species they sug- ven, Germany) and wheat flour was purchased
gested various processing techniques to improve from the supermarket (Germany). Chemical com-
palatability. Nandeesha et al. (1988) carried out position and amino acid composition of these three
an experiment in which they replaced fishmeal feed ingredients are shown in Table 1. The earth-
with earthworm Eudrilus eugeniae in diets for com- worm meal used in this trial contained more CP
mon carp, Cyprinus carpio. Dong, Guo, Ye, Song, than the fishmeal and had approximately the same
Huang and Wang (2010) studied the digestibility gross energy. The earthworm material had an
of various unconventional protein sources in tila- amino acid composition that was similar to fish-
pia, including freeze-dried earthworm meal and meal. The levels of those amino acids essential for
reported a dry matter digestibility of 98.9
fish, i.e. threonine, valine, cystine and methionine,
4.65% but did not state which species of earth- leucine, phenylalanine, histidine and arginine
worm were used. were similar or higher in earthworm meal com-
Pucher, Ngoc, Yen, Mayrhofer, El-Matboulic and pared to fishmeal. Based on the analyzed chemical
Focken (2014) showed that the tropical earth- and amino acid composition of feed ingredients
worm Perionyx excavatus can fully replace fishmeal (Table 1), four iso-nitrogenous and iso-lipidic sup-
in supplemental feeds for common carp under plemental diets were formulated at 30% of CP and
semi-intensive production conditions with fish hav- 10% of crude lipid (CL). The protein content was
ing access also to natural food resources. However, chosen to be lower than required by fish (NRC
in the study by Pucher, Ngoc, et al. (2014) it is
not possible to estimate to what extent protein
Table 1 Chemical composition and amino acid composi-
from supplemental feeds and protein from natural
tion of dry feed ingredients of the test diets
food resources contributed to the growth of fish.
For this conclusion, an estimate of the digestibility
Feed Earthworm Fish meal Wheat meal
of supplemental feed is needed. To our knowledge,
the suitability of P. excavatus has not been studied CA [% of DM] 7.3 19.1 1.8
CP [% of DM] 71.3 67.4 15.5
as a feed ingredient for common carp under con-
CL [% of DM] 7.8 12.8 1.8
trolled laboratory conditions in spite of the large GE [MJ kg1 DM] 21.4 21.6 19.3
global production of 3.7 mio tonnes of this fish Threonine [% of CP] 4.5 3.4 2.4
species in 2011 (FAO 2011). P. excavatus can be Valine [% of CP] 7.0 4.3 1.9
produced industrially using organic waste (Sinha Cys + Met [% of CP] 3.1 3.0 4.6
Isoleucine [% of CP] 4.2 3.4 2.7
et al. 2002) or at household level using ruminant
Leucine [% of CP] 7.4 6.2 5.9
manure and other available organic materials Phe + Tyr [% of CP] 7.1 5.4 6.3
(M€uller, Pucher, Tran, Focken & Kreuzer 2012). Histidine[% of CP] 2.4 2.6 2.2
The aim of this study was to test under controlled Lysine [% of CP] 6.6 6.1 2.1
laboratory conditions the digestibility and nutri- Arginine [% of CP] 6.0 5.2 3.5

tional quality of P. excavatus as a feed ingredient CA, crude ash; CL, crude lipid; CP, crude protein; Cys + Met,
in diets that are used as supplement feed in tropi- cystine + methionine; DM, dry matter; GE, gross energy;
cal pond aquaculture of common carp. Phe + Tyr, phenylalanine + tyrosine.

2918 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Aquaculture Research, 2016, 47, 2917–2927 Earthworm meal in feeds for common carp T N Ngoc et al.

2011) as they were designed to resemble diets
used by farmers in semi-intensively managed pond
culture of common carp in Vietnam where natural
food resources serve as surplus of protein for the
common carp. Under semi-intensive common carp
culture, zooplankton and macro-zoobenthos serve
as natural food resources, both being richer in pro-
tein than required by common carp (De Silva
1993; based on data by Hepher 1988; NRC
2011). Due to the higher protein supply through
natural food resources than required by common
carp, lower levels of CP and essential amino acids
in supplemental feeds are needed in fish feed (De
Silva 1993). Under this pond situation, digestible
energy becomes the first limiting factor for fish
growth and needs to be supplied to the fish within
the supplemental pellet feed (Viola 1989). The
diets were not supplemented with crystalline
amino acids, as these are typically not available
for farm-made aquafeeds in remote rural areas. No
natural food (or substitute) was offered to the fish
as this would have impeded the determination of
digestibility of the experimental diets.
The control diet was composed of fishmeal as
the main protein source, wheat meal, sunflower
oil and premixes of vitamins and minerals. In the
three treatment diets (EW30, EW70, and EW100),
30%, 70% or 100% of fishmeal protein was
replaced by earthworm protein respectively (see
Table 2). The four test feeds had similar contents
of crude ash (CA), CP, CL and gross energy (GE)
(Table 2). The content of all essential amino acids
in the experimental diets increased as the propor-
tion of earthworm increased. Titanium dioxide

Table 2 Ingredient composition of diets [% of diet DM], proximate composition, gross energy content and essential
amino acid composition [% of crude protein] of the test diets in the trial and recommended levels of common carp
(recalculated from requirements for common carp given in NRC 2011)

Feed Rec. Control EW30 EW70 EW100

Ingredient composition of diets Fishmeal [% of diet DM] 30.3 21.1 9.0 –

Earthworm [% of diet DM] – 8.8 20.2 28.7
Wheat meal [% of diet DM] 61.7 61.6 61.7 61.7
Sunflower oil [% of diet DM] 5.0 5.5 6.2 6.7
Mineral* [% of diet DM] 2.0 2.0 2.0 2.0
Vitamin† [% of diet DM] 2.0 2.0 2.0 2.0
TiO2 [% of diet DM] 1.0 1.0 1.0 1.0
Prox. composition CA [% of DM] 8.3 8.4 8.1 8.2
CP [% of DM] 27.8 27.7 27.5 27.6
DP [% of DM] 32.0‡ 22.3‡ 22.6‡ 23.5‡ 23.7‡
CL [% of DM] 9.7 9.7 9.7 9.7
GE [MJ kg1 DM] 19.4 19.4 19.4 19.4
DE [% of DM] 13.4§ 13.7§ 14.1§ 14.1§ 13.7§
Essential amino acid composition Threonine [% of CP] 3.9 3.2 3.6 4.0 4.0
Valine [% of CP] 3.7 4.0 4.3 5.1 5.8
Cys + Met [% of CP] 2.6 1.4 1.8 1.8 2.2
Isoleucine [% of CP] 2.6 3.2 3.6 4.0 4.0
Leucine [% of CP] 3.7 6.5 6.9 7.3 7.6
Phe + Tyr [% of CP] 5.3 4.0 4.0 4.4 4.3
Histidine[% of CP] 1.3 2.5 2.5 2.5 2.5
Lysine [% of CP] 5.8 5.0 5.4 5.5 5.4
Arginine [% of CP] 4.5 5.0 5.4 5.5 5.8

CA, crude ash; CL, crude lipid; CP, crude protein; Cys + Met, cystine + methionine; DE, digestible energy; DM, dry matter; DP,
digestible protein; GE, gross energy; Phe + Tyr, phenylalanine + tyrosine; Rec., Recommended content of essential amino acids;
TiO2, Titanium dioxide.
*Vitamin premix: retinol palmitate: 500 000 IU kg1; thiamine: 5 g kg1; riboflavin: 5 g kg1; niacin: 25 g kg1; folic acid:
1 g kg1; pyridoxine: 5 g kg1; cyanocobalamine: 5 g kg1; ascorbic acid: 10 g kg1; cholecalciferol: 50 000 IU kg1; a-tocoph-
erol: 2.5 g kg1; menadione: 2 g kg1; inositol: 25 g kg1; pantothenic acid: 10 g kg1; choline chloride: 100 g kg1; biotin:
0.25 g kg1.
†Mineral premix (g/k): CaCO3: 336; KH2PO4: 502; MgSO4+7 H2O: 162; NaCl: 49.8; Fe(II) gluconate: 10.9; MnSO4+H2O: 3.12;
ZnSO4+7 H2O: 4.67; CuSO4+5 H2O: 0.62; KI: 0.16; CoCl2+6 H2O: 0.08; ammonium molybdate: 0.06; NaSeO3 0.02.
‡Digestible protein calculated based on NRC (2011) for requirement and based on the results of this study (see Table 5).
§Digestible energy calculated based on NRC (2011) for requirement and based on the results of this study (see Table 5).

© 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927 2919
Earthworm meal in feeds for common carp T N Ngoc et al.
(TiO2) was added at a level of 1% to each diet as a
marker for determining digestibility according to
the equation by Bureau, Harris and Cho (1999).
Feeds were pelleted by means of a domestic meat
grinder (Bosch Comfort plus; Robert Bosch GmbH,
Gerlingen, Germany) fitted with a 1 mm die. The
pellets were dried at 40°C for 36 h and kept in the
refrigerator at 8°C.
Experimental design
The trial was carried out for 8 weeks in a recircu-
lation system that consisted of 12 aquaria of 40 L
each (four feeds 9 3 replicates). Water flow
through the aquaria was maintained at 6–
7 L min1. Water exchange rate in relation to
feed provided accounted for 5.5 m3 kg1 in the
first week and 1.9 m3 kg1 in the last week of the
experiment. Water parameters were maintained at
optimal level for common carp (temperature at
25–27°C, dissolved oxygen close to saturation and
pH around 7.0–8.0). The photoperiod was set to
12 h light: 12 h dark.
Five common carp (~8 g) were stocked ran-
domly to each aquarium. Carp were fed
16 g kg0.8, five times maintenance requirement
of 3.2 g kg0.8 metabolic body mass (Becker, Eck-
hardt & Struck 1983), equivalent to 4.2% of body
mass per day at the beginning and 3.3% of body
mass per day at the end of the experiment, divided
into five portions fed by means of automatic feed-
ers at 8, 10, 12, 14 and 16 o’clock. The pellets
sank in the water and were taken up by the fish
immediately so that leaching caused by different
palatability of feeds can be excluded. Fish growth
was monitored weekly after 24 h of starvation.
Fish faeces were collected by siphoning in all
aquaria twice a day (at 10 and 16 o’clock) in the
last 2 weeks of the trial. The collection time was
adjusted to be immediately after excretion and was
based on observations. To ensure that no feed resi-
dues remained within the faeces fraction, aquaria
were cleaned after feeding. 10–15 min after clean-
ing, faeces was siphoned into a cylinder. Settled
faeces were transferred to test tubes for centrifuga-
tion at 4000 g for 10 min. The top water layer
was poured off and the faeces was stored at
20°C before freeze-drying. This principal was per-
formed twice daily for 2 weeks. To have sufficient
amounts for analysis, faeces was pooled over the
three replicates and was analyzed in duplicates.
2920 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Aquaculture Research, 2016, 47, 2917–2927
At the end of the trial, fish were sacrificed to
determine final body weight, length of intestine,
weight of liver and proximate composition of
whole fish.
Analytical procedure
Fish were anesthetized by means of MS222
and were sacrificed by heart puncture. For
analysis, fish were homogenized and freeze-dried.
Samples of fish carcasses, feeds, feed ingredients
and fish faeces were analyzed for DM and CA
according to AOAC (1990). Total nitrogen (TN)
were determined using the Kjeldahl method
(CP = TN 9 6.25). CL was determined by extrac-
tion with a Soxlet device, and GE with bomb
calorimeter (IKA C 7000; Janke & Kunkel IKA-
Analysentechnik, Germany) using a benzoic acid
standard. The amino acid contents of the feed
ingredients and feeds were determined by the
State Agency for Agricultural Chemistry at
Hohenheim according to EU standard methods
98/64/EG and 2000/45/EG. All amino acids,
except tryptophan, were analyzed by an amino
acid analyser (Biochrom 30 & 30+; Laborservice
Onken, Greindau, Germany). Tryptophan was
analyzed by high-performance liquid chromatog-
raphy (HPLC) equipped with a fluorescence
detector.
After Kjeldahl digestion, experimental feeds and
fish faeces were treated with H2O2 and analyzed
for TiO2 by spectrophotometric absorption of
405 nm wave length. The quantity of TiO2
(lg mL1 aliquot) was computed by using the fol-
lowing equation (Richter, L€ uckst€
adt, Focken &
Becker 2003): TiO2 (lg mL1 aliquot) = 108.1 9
Abs405  0.155.
Based on these data, the following factors were
calculated:
Specific growth rate (SGR)
¼ 100  ððln final weight  ln initial weightÞ=
days of trialÞ
Condition factor (CF)
¼ ðfresh body weight [g]=body length [cm]3 Þ
 100
Hepato-somatic index (HSI)
¼ ðfresh weight of liver=fresh body weightÞ
 100
Aquaculture Research, 2016, 47, 2917–2927
Intestine-somatic index (ISI)
¼ Length of intestine=standard body length
Feed conversion ratio (FCR)
¼ feed consumption (dry matter)=
fish live weight gain
Protein productive value (PPV)
¼ 100  ðððfinal fish body proteinÞ
ðinitial fish body proteinÞÞ=
ðtotal protein consumedÞÞ
Apparent net lipid utilization (ANLU)
¼ 100  ðððfinal fish body lipidÞ
ðinitial fish body lipidÞÞ=
ðtotal lipid consumedÞÞ
Apparent net gross energy utilization (ANEU)
¼ 100  ðððfinal fish body gross energyÞ
ðinitial fish body gross energyÞÞ=
ðtotal gross energy consumedÞÞ
Apparent digestibility co-efficient of GE (E-ADC)
¼ 100
ð1  ðconc. of TiO2 in diet=conc. of TiO2 in faecesÞ
 ðGE in faeces=GE in dietÞÞ
Apparent digestibility co-efficient of CL (L-ADC)
¼ 100
ð1  ðconc. of TiO2 in diet=conc. of TiO2 in faecesÞ
 ðconc. of CL in faeces=conc. of CL in dietÞÞ
Apparent digestibility co-efficient of CP (P-ADC)
¼ 100
ð1  ðconc. of TiO2 in diet=conc. of TiO2 in faecesÞ
 ðconc. of CP in faeces=conc. of CP in dietÞÞ
Statistics
All data were tested for normal distribution and
homogeneity before statistical analysis. Results are
presented as means
SD (standard deviation).
Microsoft Excel and the program STATISTICA
(version 6, StatSoftâ, Tulsa, OK, USA) were used
for data analysis. Analysis of Variance (ANOVA) and
Tukey post-hoc tests were used to determine any
significant differences (P ≤ 0.05). Digestibility data
could not be statistically analyzed due to limited
sample availability for replication.
© 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Earthworm meal in feeds for common carp T N Ngoc et al.
Results
Feed acceptance, body condition and chemical
composition
All test diets sank quickly and were eaten very
rapidly by the fish. Therefore, the nutrient loss by
leaching was minimal due to the short time the
feed pellets remained in the water and all the feed
offered could be assumed as feed intake. No differ-
ence was observed in the acceptance of the test
diets by the fish regardless of the level of earth-
worm inclusion. No mortality occurred in the trial.
The experimental fish showed no abnormal activ-
ity at any time during the trial. All the fish
behaved normally and had similar and character-
istic shape as well as body coloration. The mor-
phometric parameters CF, HSI as well as ISI did
not show any significant differences (Table 3). Fish
fed the control diet had the highest CF and HSI
(3.41
0.13 and 2.08
0.19 respectively); fish
fed EW70 had the lowest values of these parame-
ters. ISI was highest in fish on diet EW100
(6.73
0.65) without showing significant differ-
ences to other treatments.
The proximate carcass composition of common
carp are shown in Table 4. Fish in the control
feeding group had the highest content of CL
(33.7% of DM), followed by the feeding group
EW70 (31.3% of DM). EW100 resulted in the low-
est CL content in fish with 28.6% of DM. The CP
and CA of fish carcasses in the trial fluctuated
from 58.6% to 61.5% and from 17.4% to 20.7%
of DM respectively. However, the differences in the
chemical composition between fish from the differ-
ent treatments was not statistically different
(Table 4).
Fish growth and feed utilization
The fish showed a good growth by tripling their
body mass within the 8 weeks of the trial. Fish
growth and feed utilization showed differences
between groups. Growth of fish reared on diet
EW70 had the best growth, significantly different
from all other groups (Table 3). The SGR of the
control group was lowest with 2.13% day1, fish
on EW30 (2.15
0.03% day1) and EW100
(2.18
0.04% day1) showed slightly higher
growth, and the SGR of fish on EW70
(2.29
0.01% day1) was significantly higher
than that of the other three groups (Table 3). As
2921
Earthworm meal in feeds for common carp T N Ngoc et al. Aquaculture Research, 2016, 47, 2917–2927

Table 3 Growth performance fac-

Control EW30 EW70 EW100
tors and morphometric parameters
IW [g] 8.1
0.1 8.1
0.0 8.1
0.2 8.0
0.1 (mean
standard deviation, n = 3)
FW [g] 26.6
1.1b 27.1
0.4b 29.1
0.3a 27.2
0.5b of groups of five common carp in
SGR [%] 2.13
0.06b 2.15
0.03b 2.29
0.01a 2.18
0.04b the trial
CF 3.41
0.13 3.34
0.02 3.22
0.13 3.19
0.05
HSI [%] 2.08
0.19 1.87
0.05 1.83
0.01 1.93
0.24
ISI [%] 6.36
0.55 6.22
0.14 6.32
0.11 6.73
0.65

Values in the same row with different superscript are significantly different at P ≤ 0.05.
CF, condition factor; FW, final weight; HSI, hepato-somatic index; ISI, intestine-somatic
index; IW, initial weight; SGR, specific growth rate.

Table 4 Proximate carcass compo-

Initial Control EW30 EW70 EW100
sition (mean
standard deviation,
DM [% of FM] 21.4 23.2
0.3a 22.7
0.3a 22.7
0.2a 21.5
0.3b n = 3) of common carp initial the
CP [% of FM] 13.9 13.5
0.2 13.6
0.5 13.5
0.3 13.1
0.1 trial and after feeding the different
CL [% of FM] 3.8 7.8
0.5 7.0
0.4 7.1
0.3 6.1
0.4 test diets
CA [% of FM] 3.4 2.0
0.1 2.2
0.2 2.2
0.1 2.2
0.1
GE [MJ kg1 FM] 4.7 6.1
0.3a 5.8
0.1a 5.8
0.0a 5.3
0.0b

Values in the same row with different superscript are significantly different at P ≤ 0.05.
CA, crude ash; CL, crude lipid; CP, crude protein; DM, dry matter; FM, fresh matter; GE,
gross energy.

Table 5 Utilizations of feed, crude

Control EW30 EW70 EW100
protein, crude lipid, and gross
FCR 1.32
0.08 1.26
0.05 1.22
0.02 1.27
0.02 energy (mean
standard deviation,
PPV [%] 28.0
1.2b 28.6
1.4b 31.8
1.4a 27.5
0.4b n = 3) and apparent digestibility of
ANLU [%] 69.6
8.2a 60.2
4.6ab 64.7
3.2ab 50.5
4.9b crude protein, crude lipid and gross
ANEU [%] 23.0
2.6a,b 21.0
0.9b 22.5
0.5a 18.0
1.1c energy of the test diets in common
P-ADC [%]* 80.3 81.5 85.3 85.7 carp
L-ADC [%]* 87.8 85.9 83.4 75.2
E-ADC [%]* 70.6 72.6 72.7 70.5

Values in the same row with different superscript are significantly different at P ≤ 0.05.
*Samples of the three groups per treatment were pooled and data could not be statisti-
cally analyzed due to limited sample availability.
ANEU, apparent net gross energy utilization; ANLU, apparent net lipid utilization;
E-ADC, apparent digestibility co-efficient of gross energy; FCR, feed conversion ratio;
L-ADC, apparent digestibility co-efficient of crude lipid; P-ADC, apparent digestibility
co-efficient of crude protein; PPV, protein productive value.

was the case for growth, the fish fed EW70 also
showed the lowest FCR and better results for PPV
(Table 5). Fish fed EW70 showed the highest PPV
with proximately 32%, which was significantly
higher than that of fish groups fed the other diets
(Table 5). However, there was no significant differ-
ence between the PPV of the control group, EW30
and EW100.
Apparent net lipid utilization (ANLU) was high-
est in fish fed the control diet (69.6%), and slightly
lower in the diets with earthworm inclusion. There
was no significant difference in ANLU within the
earthworm-containing diets (EW30 to EW100),
but the difference between control feed and
EW100 was significant. This group (EW100) also
had the lowest energy retention (ANEU) with only
18.0
1.1%, significantly lower than of the other
feeding groups.
Feed conversion ratios (FCRs) in this trial were
relatively low. The highest FCR was observed in
the control group (1.32
0.08), followed by
EW100 (1.27
0.02), EW30 (1.26
0.05)
while that of EW70 was the lowest (1.22
0.02).
There was no significant difference between the
control feed group and test groups for this parame-
ter (Table 5).

2922 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Aquaculture Research, 2016, 47, 2917–2927
Digestibility
In general, digestibility of all nutrients in all test
diets was high. The apparent digestibility of pro-
tein in the control feed was 80.3%, which was the
lowest protein digestibility in the trial. The protein
digestibility of feed increased proportionally to the
level of inclusion of earthworm meal. Thus, feed
EW100 had the highest apparent digestibility of
CP (85.7%), followed by EW70 (85.3%) and
EW30 (81.5%). In contrast, apparent digestibility
of lipid was inversely proportional to the amount
of earthworm meal in the feed (Table 5). Control
feed had the highest lipid digestibility (87.8%), fol-
lowed by EW30 (85.9%), EW70 (83.4%) and
EW100 (75.2%). The lipid digestibility in fully
earthworm-based feeds was lower than that of the
other test feeds. Energy digestibility was almost the
same in all diets varying from 70.5% to 72.7%.
Discussion
Experimental design
The high content of animal-based protein in the
diets (fishmeal and earthworm meal) is not typical
in supplemental feeds for pond culture of common
carp but in the context of this study, it was neces-
sary to reduce the number of feed ingredients in
order to avoid potential interactions between vari-
ous feed ingredients for the determination of
digestibility. The protein content of 30% of DM in
feeds was chosen to be less than the optimal level
for common carp (38%; NRC 2011) and the con-
tent of essential of amino acids was chosen to not
fully meet the requirements of common carp (NRC
2011). This type of feed was designed in order to
be comparable in its nutritional composition to
supplemental diets for semi-intensive pond culture
in Vietnam (e.g. Pucher, Mayrhofer, El-Matbouli &
Focken 2014; Pucher, Mayrhofer, El-Matbouli &
Focken 2016; Tuan 2010) and those used in simi-
lar experiments (e.g. Khan, Siddiqui & Nazir 1970;
Jahan, Watanabe, Kiron & Satoh 2003). Accord-
ing to De Silva (1993) and Viola (1989), digestible
energy is the first factor that is limiting fish
growth in semi-intensive aquaculture. In these
systems, digestible energy needs to be supplied by
supplemental feeds as high quality protein is avail-
able to the fish via natural food resources that are
generally rich in proteins of high quality. Subse-
quently, supplemental feeds do not need to supply
© 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Earthworm meal in feeds for common carp T N Ngoc et al.
all required nutrients as it is necessary in full feeds
for intensive aquaculture. Under pond conditions,
where natural food is available to the fish, higher
growth rates of fish can be expected. Feeding trials
with similar feeds including natural food resources
were conducted after the here described laboratory
trial (see Pucher, Ngoc, et al. 2014).
Nutritional quality of earthworm
In our study, the earthworm P. excavatus had a
higher protein content than that of conventional
fishmeal (Hertrampf & Piedad-Pascual 2000) and
that of the fishmeal been used in this trial. Further,
the protein content of P. excavatus was higher than
in most other earthworm species that were evalu-
ated by Tacon et al. (1983), Tacon and Jackson
(1985), Hilton (1983), and Stafford and Tacon
(1984). Similarly, the content of essential amino
acids in P. excavates was comparable to or higher
than that of conventional fishmeal (Hertrampf &
Piedad-Pascual 2000) and that of the fishmeal used
in this trial. The essential amino acid composition
of earthworm differs from species to species (Dynes
2003), culture environment, and substrate quality
(Xiang, Zhang, Pan, Qiu & Chu 2006). Compared to
the amino acid profile of the earthworm species
Lumbricus rubellus, L. terrestris, Nicodrilus roseus,
N. caliginosus, Dendrobawna octaedra, Eisenia norden-
skioldi, Octolasium lacteum, Drawida ghilarovi and
Hyperiodrilus euryaulos, which were investigated by
Pokarzhevskii, Zaboyev, Ganin and Gordienko
(1997) and Sogbesan, Ugwumba and Madu
(2007), P. excavatus showed a profile of essential
amino acids that was one of the better profiles fit-
ting to the requirements of common carp. Espe-
cially, P. excavatus showed higher concentration of
methionine and cystine (3.1% of CP) than most
other earthworm species (<2% of CP: Pokarzhevskii
et al. 1997). These sulphur-containing amino acids
are usually among the most limiting amino acids in
aquafeeds. We found in our study that P. excavatus
seems to be a suitable source of essential amino
acids as an increasing portion of protein from earth-
worm resulted in a higher content of almost all
essential amino acids in the diets.
Perionyx excavatus had a lower lipid content
than fishmeal. So far, not many publications are
available on lipid composition of earthworms,
especially no one for P. excavatus. Paoletti, Bus-
cardo, VanderJagt, Pastuszyn, Pizzoferrato, Huang,
Chuang, Millson, Cerda, Torres and Glew (2003)
2923
Earthworm meal in feeds for common carp T N Ngoc et al.
reported that two earthworm species (Andiorrhinus
kuru, Andiorrhinu motto) appeared to contain insuf-
ficient amounts of triacyglycerols which are impor-
tant as energy stores in cells. Holmstrup,
Sørensen, Bindesbøl and Hedlund (2007) showed
that the earthworm Dendrobaena octaedra contained
high amounts of long-chain unsaturated fatty
acids (20:n and 18:n). Thus, the composition of
fatty acids in earthworms seems to be complex
and differs from species to species. However, the
quality of lipids in earthworm meal should be con-
sidered more in detail in future research as the
results in this study suggest an interaction of
earthworm-protein and lipids in their effect on
growth, digestibility and utilization efficiency.
Digestibility
In our study, increased levels of earthworm in the
diets led to proportional reductions of lipid digest-
ibility and CL content in fish. Apparent net lipid
utilization (ANLU) showed that full replacement
achieved a significantly lower lipid utilization and
the lowest CL content in fish carcass. This might
be caused by the increasing substitution of fish
lipid originating from fishmeal through sunflower
oil in feeds with increasing earthworm meal con-
tent. Therefore, substitution by fish oil rather than
by sunflower oil might improve fish growth as dis-
cussed previously (Nandeesha et al. 1988). In
future studies, an analysis of the fatty acids in
earthworm P. excavatus might give more detailed
insight into the suitability of earthworm meal not
only as an animal protein source but also as a
source of essential fatty acids for fish. The appar-
ent digestibility of energy (E-ADC) in groups fed by
the control and EW100 were lowest while the
energy digestibility was highest in the EW70
group. Contrarily, the apparent net gross energy
utilization (ANEU) was highest in groups fed the
control and EW70 diet. Significantly lowest ANEU
was detected in the EW100 group. This pattern
might suggest changes in the utilization of lipids
and proteins in feeds as energy sources for fish.
The digestibility of protein increased proportion-
ally with increasing earthworm meal content in
feeds. But due to large variation between the
duplicated analyses, any difference in digestibility
could be detected. Higher replication might be ben-
eficial to show the significant difference in earth-
worm protein digestibility. Even though the
apparent protein digestibility was highest in
2924 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Aquaculture Research, 2016, 47, 2917–2927
EW100, the digested protein contributed to a
lower content to the body mass gain as the PPV
dropped significantly in the EW100 group com-
pared to the EW70 which was the group with
highest PPV. The PPV in the control group were
similar to the EW30 and EW100 groups.
Growth performance
The increase in earthworm content in feeds
improved proportionally the growth performance
and feed conversion up to the replacement of 70%
fishmeal-protein by earthworm-protein. Groups fed
by EW70 showed the highest growth rates (SGR of
2.3% day1) and lowest FCRs (1.22) of all tested
feeds. The full replacement of fishmeal by earth-
worm meal resulted in a drop in growth and feed
utilization, even though the test diet EW100 had a
higher content of essential amino acids and the
protein digestibility of earthworm meal was found
to be highest in the EW100 feed. This indicates
that the lower growth rate of fish fed EW100 was
not directly linked to the quality of the earthworm
protein but may have been caused by other factors.
There seems to be a synergetic effect of combining
earthworm and fishmeal or other animal derived
proteins sources (e.g. natural food resources as
shown by Pucher, Ngoc, et al. 2014). Earlier stud-
ies (Tacon et al. 1983; Stafford & Tacon 1984;
Nandeesha et al. 1988) also reported that total
replacement of fishmeal by earthworm meal did
not result in the highest growth even though
earthworm has a better nutritive profile. In the
trial by Nandeesha et al. (1988), the best feed was
the one containing 25% earthworm. However, this
result could be strongly influenced by the addition
of 5% of sardine oil in the diet as Espe, Lemme,
Petri and El-Mowafi (2006) implied that a few per
cent of fish oil in the diet could improve palatability
of feeds and lead to higher feed intake and fish
growth. In our study, fish grew best with 70% of
fishmeal-CP replacement. This level is equivalent to
20% of DM and agrees with earlier studies (Hilton
1983; Tacon et al. 1983; Nandeesha et al. 1988).
Tacon et al. (1983) claimed that the best fish
growth could be achieved with lower than 30%
fishmeal replacement by earthworm.
Hilton (1983) stated that diets containing earth-
worm meal reduced feed intake and growth. Sev-
eral suggestions have been made by researchers to
explain why earthworm meal based diets reduce
growth rates. Tacon et al. (1983), Andrews and
Aquaculture Research, 2016, 47, 2917–2927
Kukulinsky (1975), and Edwards and Lofty (1977)
reported that the coelomic fluid, a yellow fluid in
earthworms, could make feeds unpalatable when
they contained large amounts of earthworm and
could thus decrease feed intake. Coelomic fluid
contains specific proteins that affect the immune
system of other animals (Kauschke, Mohrig & Coo-
per 2007). Proper pre-treatment (e.g. heat treat-
ment) of earthworm before using them in fish
diets might improve the palatability of earthworm
meal (Tacon et al. 1983; Pucher, Ngoc, et al.
2014). In the study of Nandeesha et al. (1988),
earthworm was cooked before pelletization. Never-
theless, total fishmeal replacement by heat-treated
earthworm did not achieve higher growth than
the feed with 25% earthworm inclusion in the
study by Nandeesha et al. (1988). This indicates
that the heat treatment of earthworm by Nandee-
sha et al. (1988) did not destroy the anti-nutri-
tional factor. Further research is needed to
investigate the existence of potential anti-nutri-
tional factors in certain earthworm species and the
proper pre-treatment to reduce the anti-nutritional
property.
There is the possibility, that earthworms been
used in the research trials might be cultured on
waste materials that contain heavy metals, deter-
gents and other undesirable compounds. Some
researchers reported accumulation of chemicals
such as fluoride in earthworm living in polluted
soils (Vogel & Ottow 1991) or iron, zinc, lead, and
cadmium (Stafford & Tacon 1984; Paoletti et al.
2003; Khwairakpam & Bhargava 2009). Stafford
and Tacon (1984) pointed out that these materials
can contaminate the diets and impair fish perfor-
mance at high levels of earthworm incorporation.
Consequently, vermiculture must be well managed
by assuring a high quality of feeds and environ-
ment if earthworm is to be used in animal feeds.
In summary, common carp have shown very
good growth response to feeds containing earth-
worm meal as the main protein source. For practi-
cal purposes, the use of earthworm meal in mainly
plant-based feeds also needs to be evaluated. If
found to be suitable for these feeds, too, earth-
worm meal can become a source of animal protein
for farm-made as well as commercial aquafeeds.
Acknowledgments
This study was partly funded by the Deutsche
Forschungsgemeinschaft (DFG) and was carried
© 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2917–2927
Earthworm meal in feeds for common carp T N Ngoc et al.
out under the umbrella of the Uplands Program
(SFB 564) in close collaboration between the Uni-
versity of Hohenheim (Germany) and the Hanoi
University of Agriculture (Vietnam). A scholarship
awarded by the Deutsche Akademische Auslandsd-
ienst (DAAD) to Tuan NN is gratefully acknowl-
edged. Special thanks go to Dr. Lawrence for the
language editing of this article and to the review-
ers for their constructive comments.
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