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SPRINGER BRIEFS IN MOLECULAR SCIENCE
CHEMISTRY OF FOODS

Laura Gasco · Francesco Gai

Giulia Maricchiolo
Lucrezia Genovese · Sergio Ragonese
Teresa Bottari · Gabriella Caruso

Feeds for the

Aquaculture
Sector
Current Situation
and Alternative
Sources
SpringerBriefs in Molecular Science

Chemistry of Foods

Series editor
Salvatore Parisi, Industrial Consultant, Palermo, Italy
The series Springer Briefs in Molecular Science: Chemistry of Foods presents
compact topical volumes in the area of food chemistry. The series has a clear focus
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overview on the chemistry related to specific topics in this area. Typical topics thus
include: - Compound classes in foods – their chemistry and properties with respect
to the foods (e.g. sugars, proteins, fats, minerals, …) - Contaminants and additives
in foods – their chemistry and chemical transformations - Chemical analysis and
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More information about this series at http://www.springer.com/series/11853

Laura Gasco Francesco Gai
•

Giulia Maricchiolo Lucrezia Genovese

•

Sergio Ragonese Teresa Bottari

•

Gabriella Caruso

Feeds for the Aquaculture

Sector
Current Situation and Alternative Sources

123
Laura Gasco Sergio Ragonese
Department of Agricultural, Forest, Institute for Coastal Marine
and Food Sciences Environment—CNR
University of Turin Mazara del Vallo (TP)
Grugliasco Italy
Italy
Teresa Bottari
Francesco Gai Institute for Coastal Marine
Institute of Food Production Environment—CNR
Sciences—CNR Messina
Grugliasco Italy
Italy
Gabriella Caruso
Giulia Maricchiolo Institute for Coastal Marine
Institute for Coastal Marine Environment—CNR
Environment—CNR Messina
Messina Italy
Italy

Lucrezia Genovese
Institute for Coastal Marine
Environment—CNR
Messina
Italy

ISSN 2191-5407 ISSN 2191-5415 (electronic)

SpringerBriefs in Molecular Science
ISSN 2199-689X ISSN 2199-7209 (electronic)
Chemistry of Foods
ISBN 978-3-319-77940-9 ISBN 978-3-319-77941-6 (eBook)
https://doi.org/10.1007/978-3-319-77941-6

Library of Congress Control Number: 2018934949

© The Author(s) 2018

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Contents

1 Fishmeal Alternative Protein Sources for Aquaculture Feeds . . . . .. 1

Laura Gasco, Francesco Gai, Giulia Maricchiolo, Lucrezia Genovese,
Sergio Ragonese, Teresa Bottari and Gabriella Caruso
1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 Insect Meals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
1.2.1 Tenebrio Molitor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
1.2.2 Hermetia Illucens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
1.2.3 Musca Domestica . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
1.3 Poultry by-Product Meals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
2 Fishery Discard as a Source of Food for Reared or Wild Fish?
The Bottom Trawling in the Mediterranean Sea
as a Case Study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 29
Laura Gasco, Francesco Gai, Giulia Maricchiolo, Lucrezia Genovese,
Sergio Ragonese, Teresa Bottari and Gabriella Caruso
2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
2.2 Discards in the Mediterranean Sea . . . . . . . . . . . . . . . . . . . . . . . . 30
2.3 Impact of Discards on Ecosystem . . . . . . . . . . . . . . . . . . . . . . . . 32
2.4 Management Actions and Tools . . . . . . . . . . . . . . . . . . . . . . . . . 34
2.5 Use of ‘Recovered’ Discards in Aquaculture . . . . . . . . . . . . . . . . 35
2.6 Case Study: Bottom Trawling off South of Sicily
(GSA 16–Central Mediterranean) . . . . . . . . . . . . . . . . . . . . . . . .. 37
2.7 Discussion of the Case Study . . . . . . . . . . . . . . . . . . . . . . . . . .. 42
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 43
3 Sustainable Alternatives for Dietary Fish Oil in Aquafeeds:
Actual Situation and Future Perspectives . . . . . . . . . . . . . . . . . . . . . 49
Laura Gasco, Francesco Gai, Giulia Maricchiolo, Lucrezia Genovese,
Sergio Ragonese, Teresa Bottari and Gabriella Caruso

v
vi Contents

3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........ 49

3.2 Effects of Dietary Plant Oils on the Nutritional Quality
of Farmed Salmonids . . . . . . . . . . . . . . . . . . . . . . . . . ........ 51
3.3 Effects of Dietary Plant Oils on the Nutritional Quality
of Farmed Mediterranean Marine Fish . . . . . . . . . . . . . . . . . . . . . 52
3.4 Future Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
3.5 Closing Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
4 Supplementation of Vitamins, Minerals, Enzymes and
Antioxidants in Fish Feeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 63
Laura Gasco, Francesco Gai, Giulia Maricchiolo, Lucrezia Genovese,
Sergio Ragonese, Teresa Bottari and Gabriella Caruso
4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
4.2 Vitamins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
4.2.1 Water-Soluble Vitamins . . . . . . . . . . . . . . . . . . . . . . . . . . 66
4.2.2 Fat-Soluble Vitamins (Vitamin A, D, E and K) . . . . . . . . . 76
4.3 Minerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
4.3.1 Macrominerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
4.3.2 Microminerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
4.4 Enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
4.5 Probiotics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
4.6 Antioxidants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93
4.7 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
Abbreviations

ADC Apparent digestibility coefficient

ALA Alpha-linolenic acid
BI Biomass index
BM Blood meal
Ca Calcium
CFP Common Fisheries Policy
CFU Colony forming unit
CP Crude protein
CPO Crude palm oil
Cr Chromium
CRS Catch returned to the sea
Cu Copper
DHA Docosahexaenoic acid
DI Density index
DM Dry matter
EAA Essential amino acid
EE Ether extract
EFA Essential fatty acids
EFSA European Food Safety Authority
EOLSS Encyclopaedia of Life Support Systems
EPA Eicosapentaenoic acid
EU European Union
FA Fatty acids
FAD Flavin adenine dinucleotide
FAO Food and Agriculture Organization of the United Nations
FCR Feed conversion rate
Fe Iron
FI Feed intake
FM Fishmeal
FMN Flavin mononucleotide

vii
viii Abbreviations

FO Fish oil
FR Feeding rate
GFCM General Fisheries Commission for the Mediterranean Sea
GSA Geographical sub-area
HI Hermetia illucens
HUFA Highly unsaturated fatty acid
ISSFAL International Society for the Study of Fatty Acids and Lipids
LA Linoleic acid
LAB Lactic acid bacteria
Lc Length at capture
LC-HUFA Long chain-highly unsaturated fatty acids
LC-PUFA Long chain-polyunsaturated fatty acids
LCRS Landed catch returned to the sea
Lm50% Length at sexual maturity
LO Linseed oil
MBM Meat and bone meal
MCS Minimum conservation size
MD Musca domestica
MEDITA Mediterranean International Bottom Trawl Survey
Mg Magnesium
Mn Manganese
NAD Nicotinamide adenine dinucleotide
NADP Nicotinamide adenine dinucleotide phosphate
NRC National Research Council
OA Oleic acid
P Phosphorus
PAP Processed animal proteins
PBM Poultry by-product meal
PER Protein efficiency rate
PO Plant oil
PUFA Polyunsaturated fatty acid
RO Rapeseed oil
SAUP Sea Around Us Project
SBM Soybean meal
SBO Soyabean oil
SFA Saturated fatty acids
SGR Specific growth rate
SIBM Società Italiana di Biologia Marina
STECF Scientific, Technical and Economic Committee for Fisheries
TL Total length
TM Tenebrio molitor
TW Total weight
WBC Whole body composition
WG Weight gain
Zn Zinc
Chapter 1
Fishmeal Alternative Protein Sources
for Aquaculture Feeds

Laura Gasco, Francesco Gai, Giulia Maricchiolo, Lucrezia Genovese,

Sergio Ragonese, Teresa Bottari and Gabriella Caruso

Abstract Aquaculture currently accounts for approximately 50% of fish consumed

by humans. The future development of aquaculture will be greatly constrained by
the increasing costs of fishmeal and fish oil. To remedy this situation, scientific
research and feed manufacturers have made a significant progress by looking for
alternative protein sources for use in fish diets in order to develop feeds that provide
adequate nutrition for animals’ growth, while reducing to minimum the use of
traditional sources of protein. This chapter aims at critically reviewing recent
studies, carried out worldwide, about the effects of the inclusion of new protein
sources as insect, poultry by-products, meat and bone meals and other protein
sources alternative to fishmeal in aquafeeds. In particular, the impacts of these
protein sources in terms of growth, nutrient digestibility, fillet quality traits and
sensorial perception in the most important farmed marine and freshwater fish
species are evaluated.

Keywords Alternative proteins Aquaculture Fishmeal

Insects


Poultry By-Products Processed animal proteins

1.1 Introduction

The global demand for fish products is expected to increase significantly in the next
35 years due to the increase in world population that, according to the last Food and
Agriculture Organization of the United Nations (FAO) evaluations, will reach 9.5
billion people in 2050 (FAO 2016). Although there is a slight improvement in the
state of certain fish stocks due to improved fisheries management, the expected
increase will be possible only through aquaculture production that already provides
half of all seafood for human consumption (FAO 2016). Aquaculture is claimed to
be the fastest growing food production sector in the world. Fish from fisheries and

L. Gasco et al. Chemistry of Foods: Feeds for the Aquaculture Sector—Current Situation and
Alternative Sources, SpringerBriefs in Chemistry of Foods.

© The Author(s) 2018 1

L. Gasco et al., Feeds for the Aquaculture Sector, Chemistry of Foods
https://doi.org/10.1007/978-3-319-77941-6_1
2 1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

aquaculture provide important nutrients (energy, protein, vitamins and minerals)

and fish supply reached a new record of about 20 kg in 2014 accounting for about
17% of the global population’s intake of animal protein and 6.7% of all consumed
proteins (FAO 2014).
While in the past, aquaculture feeds largely used fishmeal (FM) and fish oil
(FO), these ingredients are no longer sustainable (Hardy 2010; Oliva-Teles et al.
2015; Tacon and Metian 2008). Moreover, these resources experienced periodic
fluctuations in availability and pricing. Nowadays, their inclusion is reduced to the
minimum amount able to cover the optimal content of amino acids and other
nutrients needed for fish growth and flesh quality; sometimes, aquafeed industry
produces fish diets that are completely free of these marine ingredients. Plant
feedstuffs are widely used as an alternative to FM as they are available in large
quantities when compared to FM (Gatlin et al. 2007; Naylor et al. 2009; Oliva-Teles
et al. 2015). Nevertheless, in carnivorous fish species, the complete substitution of
FM is still a challenge and its complete elimination is still associated with reduced
performances and fish health (Desai et al. 2012; Krogdahl et al. 2010; Oliva-Teles
et al. 2015). Moreover, in recent years, plant proteins for fish feeds face problems of
increasing price and of competition with other sectors as human consumption,
animal husbandry sector or biodiesel production (Moutinho et al. 2017; Pinotti et al.
2014). The use of terrestrial processed animal proteins (PAP) such as blood meal
(BM), meat and bone meal (MBM), feather meal and poultry by-product meal
(PBM) in aquaculture feeds is a common practice.
PAP have high protein and lipid content which make them very interesting for
the formulation of cost-effective aquaculture feeds. PAP are a natural source of
several nutrients such as amino acids (lysine, sulphur amino acids, histidine and
arginine) or phosphorus. They are relatively free from any anti-nutritional factor,
result to be highly palatable to most fish species, and their inclusion in aquafeeds
complement very well certain plant protein ingredients (Bureau 2006).
Nevertheless, the inclusion levels are limited by fish species, poor digestibility,
deficiency of some essential amino acids (EAA) and general nutritional quality that
highly depend on the raw material composition, freshness and processing condi-
tions (Bureau et al. 1999, 2000; Goda et al. 2007). The use of PAP is highly
depending on the considered region of the world. For instance, following the bovine
spongiform encephalopathy emergency, European Union (EU) prohibited the use of
PAP (EC No 999/2001). In 2013, this ban was partially lifted (EC No 56/2013), and
the use of PAP from non-ruminant animals (poultry and pigs) (category 3) was
reintroduced in fish feeds. Recently, the European Commission approved the use of
PAP from seven insect species in aquafeed with the Regulation 2017/893/EC.
In the following paragraphs, different alternative protein sources investigated in
field trials on cultured fish species as well as their effects on growth, nutrient
digestibility, fillet quality traits and sensorial perception are reported and
commented.
1.2 Insect Meals 3

1.2 Insect Meals

The potential use of insect meal in fish diets has recently attracted much attention
(Barroso et al. 2014; Henry et al. 2015). Carnivorous fish already count insects as
part of their natural diet (Henry et al. 2015). It seems therefore reasonable to
consider insect meals as raw material in fish feeds. Following the European Food
Safety Authority (EFSA) scientific opinion on the use of insects as food and feed,
the Standing Committee on Plants, Animals, Food and Feed has approved recently
the draft of the Regulation amending Annexes I and IV to Regulation (EC) No 999/
2001 and of the Council and Annexes X and XV to Commission Regulation
(EC) No 142/2011 as regards the provisions on processed animal protein. The use
of insect-derived PAP in aquafeeds in Europe is allowed since July 2017
(Commission Regulation (EU) 2017/893 of 24 May 2017).
In EU, the authorized insect meal is only those obtained from: (i) Hermetia
illucens (HI, Black Soldier Fly) and Musca domestica (MD); (ii) Tenebrio molitor
(TM, Yellow Mealworm) and Alphitobius diaperinus (Lesser Mealworm);
(iii) Acheta domesticus (House cricket), Gryllodes sigillatus (Banded cricket) and
Gryllus assimilis (Field Cricket). Nevertheless, in countries other than EU, rules
could be different and other insects are considered as very interesting for fish
nutrition (Barroso et al. 2014; Henry et al. 2015; Makkar et al. 2014).
When considering insects and FM ingredients for fish feeds, not only aspects
such as energy, protein and EAA, fat or mineral content and many other chemical
data (Tables 1.1, 1.2 and 1.3) have to be considered but also the raw material
availability. In this sense, only few insect species so far have the potential to be
produced in large scale and thus have received much attention as aquaculture feeds
namely TM, HI and MD.
The chemical composition and the nutritional value of insect larvae meals
(Table 1.1) largely depend on the treatment (i.e. drying methodologies, defatting
procedures) and on the substrate used to rear them (Henry et al. 2015). In particular,
while the protein content does not vary to a large extent due to the rearing substrate,
the lipid fraction is the most susceptible to changes, both from a quantitative and
qualitative fatty acid (FA) profile point of view (Henry et al. 2015; Makkar et al.
2014). As far as gross energy is considered, insect larvae meals have contents greater
than 21 MJ kg/dry matter (DM). The high insect larvae fat content (15–50%) can
sometimes cause problems. In fact, their inclusion as protein source automatically
brings also a high fat content that can generate problems both for feed formulation
but also for storage and pellet stability. For these reasons, insect producers consider
defatting process using various methods (physical or chemical extractions). In this
case, the percentage of protein (and consequently of EAA) is greatly increased and
the extracted oils may be used for other purposes such as feed inclusion (Schiavone
et al. 2017) or biodiesel production (Henry et al. 2015; Li et al. 2016; Surendra et al.
2016). As far as EAA are concerned (Tables 1.1, 1.2 and 1.3), the profiles of HI and
MD are considered close to FM profiles while the one of TM closer to that of SBM.
 4

Table 1.1 Nutrient composition and nutritive value of most promising insect larvae meals compared to fishmeal (FM) and soybean meal (SBM). Values are
reported as mean of values found in the cited references (in parenthesis minimum and maximum values). The following chemical values are shown here: dry
matter (DM), crude fibre, crude protein, lysine, methionine, sum of methionine and cysteine, tryptophan, threonine, leucine, isoleucine, valine, histidine,
arginine and the sum of phenylalanine and tyrosine
Unit Tenebrio molitora Hermetia illucensb Musca domesticac FMd SBMe
Dry Matter (DM) % as fed 42.2 (37.1–57.6) 91.3 (90.0–92.5) 92.4 (90.0–94.7) 92.1 (90.0–94.4) 87.9 (85.0–92.1)
Crude fibre % DM 5.9 (5.0–6.9) 7.0 14.7 (1.6–29.7) – 6.7 (3.5–10.1)
Crude protein % DM 51.5 (44.1–60.3) 49.1 (35.5–72.5) 49.9 (37.5–63.8) 75.6 (70.2–80.7) 51.4 (48.3–54.5)
Lysine % protein 4.5 (1.7–6.1) 6.4 (5.6–8.0) 6.1 (4.4–8.2) 6.1 (5.5–7.5) 6.1 (5.7–6.6)
Methionine % protein 1.5 (1.2–2.0) 1.8 (1.4–2.4) 2.3 (1.3–3.7) 2.2 (2.0–2.6) 1.4 (1.2–1.6)
Methionine + Cystine % protein 2.3 (1.8–2.9) 2.2 (1.5–3.1) 3.0 (1.7–4.7) 2.9 (2.6–3.2) 2.9 (2.5–3.3)
Tryptophan % protein 0.9 (0.0–1.8) 0.8 (0.5–1.1) 1.8 (1.4–3.2) 0.8 (0.7–0.9) 1.3 (1.2–1.4)
Threonine % protein 3.6 (2.7–4.4) 3.6 (1.3–4.8) 3.8 (2.0–7.6) 3.1 (2.9–4.3) 3.9 (3.5–4.3)
Leucine % protein 7.6 (4.5–10.6) 7.3 (6.6–8.4) 5.7 (4.5–6.4) 5.9 (5.2–7.3) 7.5 (6.8–8.0)
Isoleucine % protein 4.1 (2.6–5.0) 4.7 (4.0–5.6) 2.9 (1.7–3.7) 3.7 (3.3–4.4) 4.6 (4.3–5.0)
Valine % protein 5.5 (3.7–6.6) 6.9 (5.6–9.1) 3.3 (1.3–4.9) 4.2 (3.9–4.8) 4.8 (4.3–5.4)
Histidine % protein 3.0 (2.1–3.6) 3.1 (2.3–4.5) 3.0 (1.0–5.1) 1.8 (1.7–1.9) 2.6 (2.4–2.9)
Arginine % protein 4.5 (3.6–5.6) 5.4 (4.8–6.1) 4.9 (3.7–5.8) 4.6 (4.0–6.0) 7.4 (6.8–8.1)
Phenylalanine + tyrosine % protein 10.7 (8.6–12.1) 11.2 (9.6–13.3) 9.8 (6.2–17.3) 5.5 (5.2–6.5) 8.5 (7.7–9.4)
a
Data from Barroso et al. (2014), Feedpedia: http://www.feedipedia.org, Gasco et al. (2016), Marono et al. (2015), Sánchez-Muros et al. (2015), Siemianowska
et al. (2013)
b
Data from Diener et al. (2009), Feedpedia: http://www.feedipedia.org, Józefiak et al. (2016), Makkar et al. (2014), Maurer et al. (2016), Marono et al. (2015),
Sánchez-Muros et al. (2015), Tschirner and Simon (2015)
c
Data from Aniebo et al. (2008), Aniebo and Owen (2010), Barroso et al. (2014), Feedpedia: http://www.feedipedia.org; Fasakin et al. (2003), Józefiak et al.
(2016), Makkar et al. (2014), Sanchez-Muros et al. (2015), Sogbesan et al. (2006), Tschirner and Simon (2015), Zuidhof et al. (2003)
d
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
e
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
1 Fishmeal Alternative Protein Sources for Aquaculture Feeds
 1.2 Insect Meals

Table 1.2 Nutrient composition and nutritive value of most promising insect larvae meals compared to fishmeal (FM) and soybean meal (SBM). Values are
reported as mean of values found in the cited references (in parenthesis minimum and maximum values). The following chemical values are shown here: ether
extract, saturated fatty acids (FA), monosaturated FA, n6-polyunsaturated FA and n3-polyunsaturated FA
Unit Tenebrio molitora Hermetia illucensb Musca domesticac FMd SBMe
Ether extract % DM 30.2 (16.6–43.1) 20.0 (3.4–38.6) 15.8 (6.3–31.3) 8.1 (2.0–12.0) 2.1 (2.0–2.2)
Saturated fatty acids (FA) % Total FA 26.4 (22.2–35.1) 33.3 41.3 (33.1–49.2) 19.5 (18.9–19.7) 15.1 (14.9–15.2)
Monosaturated FA % Total FA 41.7 (35.1–51.5) 43.4 38.9 50.8 (50.5–52.1) 21.1 (20.5–21.7)
n6 Polyunsaturated FA % Total FA 25.5 (11.5–34.5) 15.0 18.4 1.8 (1.8–2.0) 56.1 (55.9–56.3)
n3 Polyunsaturated FA % Total FA 1.1 (0.8–1.4) 8.3 – 8.1 (2.0–12.0) 2.1 (2.0–2.2)
a
Data from Barroso et al. (2014), Feedpedia: http://www.feedipedia.org, Gasco et al. (2016), Marono et al. (2015), Sánchez-Muros et al. (2015), Siemianowska
et al. (2013)
b
Data from Diener et al. (2009), Feedpedia: http://www.feedipedia.org, Józefiak et al. (2016), Makkar et al. (2014), Maurer et al. (2016), Marono et al. (2015),
Sánchez-Muros et al. (2015), Tschirner and Simon (2015)
c
Data from Aniebo et al. (2008), Aniebo and Owen (2010), Barroso et al. (2014), Feedpedia: http://www.feedipedia.org, Fasakin et al. (2003), Józefiak et al.
(2016), Makkar et al. (2014), Sanchez-Muros et al. (2015), Sogbesan et al. (2006), Tschirner and Simon (2015), Zuidhof et al. (2003)
d
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
e
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
5
 6

Table 1.3 Nutrient composition and nutritive value of most promising insect larvae meals compared to fishmeal (FM) and soybean meal (SBM). Values are
reported as mean of values found in the cited references (in parenthesis minimum and maximum values). The following values are shown here: minerals (ash),
calcium, phosphorus, sodium, potassium, magnesium and gross energy
Unit Tenebrio molitora Hermetia illucensb Musca domesticac FMd SBMe
Minerals (ash) % DM 3.8 (1.0–6.5) 13.6 (4.3–28.4) 11.4 (5.0–23.1) 16.6 (12.0–23.3) 6.9 (6.8–7.0)
Calcium g/kg DM 2.7 (0.3–6.2) 75.6 (50.0–86.3) 4.7 (3.1–8.0) 36.3 (15.4–78.3) 3.9 (2.3–6.3)
Phosphorus g/kg DM 7.8 (4.4–14.2) 9.0 (6.4–15.0) 16.0 (9.7–24.0) 25.9 (19.0–40.4) 6.9 (5.8–8.6)
Sodium g/kg DM 0.9 1.3 5.2 (2.8–8.6) 10.0 (5.9–14.4) 0.1 (0.0–0.8)
Potassium g/kg DM 8.9 (8.5–9.3) 6.9 5.7 (1.0–12.7) 10.2 (5.9–14.4) 23.7 (21.8–26.0)
Magnesium g/kg DM 2.3 (2.0–2.8) 3.9 3.4 (0.7–11.5) 2.5 (1.6–3.1) 3.1 (2.4–3.6)
Gross energy MJ/kg DM 26.2 (24.4–28.7) 22.8 (21.2–24.4) 21.7 (19.3–24.4) 21.4 (19.6–23.8) 19.9 (19.8–20.0)
a
Data from Barroso et al. (2014), Feedpedia: http://www.feedipedia.org, Gasco et al. (2016), Marono et al. (2015), Sánchez-Muros et al. (2015), Siemianowska
et al. (2013)
b
Data from Diener et al. (2009), Feedpedia: http://www.feedipedia.org, Józefiak et al. (2016), Makkar et al. (2014), Maurer et al. (2016), Marono et al. (2015),
Sánchez-Muros et al. (2015), Tschirner and Simon (2015)
c
Data from Aniebo et al. (2008), Aniebo and Owen (2010), Barroso et al. (2014), Feedpedia: http://www.feedipedia.org, Fasakin et al. (2003), Józefiak et al.
(2016), Makkar et al. (2014), Sanchez-Muros et al. (2015), Sogbesan et al. (2006), Tschirner and Simon (2015), Zuidhof et al. (2003)
d
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
e
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
1 Fishmeal Alternative Protein Sources for Aquaculture Feeds
1.2 Insect Meals 7

Deficiencies in lysine or methionine (Barroso et al. 2014; Henry et al. 2015) are
reported.
TM larvae meals evaluated so far have a protein content varying from 44 to
60%. The lipid fraction (about 16.6 to 43% DM) is characterized by high levels of
oleic (42.18% fatty acid—FA), linoleic (24.70% FA) and palmitic (18.42% FA)
acids. The low ash content (about 3.8% DM) is very interesting for the aquaculture
sector even if TM larvae are usually low in calcium. Nevertheless, it has been
highlighted that their calcium content can be modified through the rearing substrate
(Anderson 2000; Klasing et al. 2000), increasing the level of this important mineral
in meals.
The protein content of HI larvae meals evaluated in different research varied
between 35.30 and 72.50% of DM. This high variation can be justified by the
availability on the market of several different defatted HI meals. The processing and
extraction of part of the lipid fraction from HI larvae generates protein meals having
lipid content that varied from 3.4 to 38.6% of DM. The FA profile of HI meals use
to be characterized by high values of lauric acid as, independently from the used
substrate, larvae neo-synthesized and accumulated this FA (Spranghers et al. 2016).
HI meals are rich in ash, calcium and phosphorus (Makkar et al. 2014; Tschirner
and Simon 2015). MD larvae meals have a protein and lipid content ranging from
37.5 to 63.8% of DM and from 6.28 to 31.30% of DM, respectively (Aniebo and
Owen 2010; Barroso et al. 2014; Józefiak et al. 2016; Makkar et al. 2014;
Sánchez-Muros et al. 2014; Sogbesan et al. 2006; Zuidhof et al. 2003). The main
reported FA are palmitic (32.37% FA), oleic (21.96% FA), linolenic (19.70% FA)
and palmitoleic (17.10% FA) acids. The calcium content (about 4.7 g/kg DM) is
higher than that of the TM larva but lower than that of HI (Makkar et al. 2014).
When compared to conventional protein sources (FM or soybean meal—SBM),
the insect larvae protein content is lower than that of the FM (66–72%) but similar
or higher than SBM (44–50%). With regard to the lipid content, insect larvae used
to have higher values than conventional sources. Larvae contain between 8 and
36% of nitrogen-free extracts (sugars, starch, chitin and fibrous fractions) (Barroso
et al. 2014).
As far as the lipid profile is concerned, insect larvae are poor in highly unsat-
urated fatty acids. The main difference between insect meals and FM is the content
of eicosapentaenoic acid (EPA, C20:5 n3) and docosahexaenoic acid (DHA, C22:6
n3) which are present in the marine and freshwater products, but are absent in
land-based products (including SBM) and insects. Usually, increasing levels of
insect meal inclusion lead to a dramatic change of the FA profile in fish with a
decrease in EPA and DHA and a decrease in the n3/n6 fatty acid ratio (Belforti et al.
2015; Gasco et al. 2016; St-Hilaire et al. 2007a, b). Nevertheless, it is possible to
increase the insect unsaturated FA content manipulating the rearing substrate
(Belforti et al. 2014; St-Hilaire et al. 2007a). In particular, while the fatty acids of
HI pre-pupae reared on cow manure were high in saturated fatty acids (SFA) and
very low in poly-unsaturated FA n3 (0.2%), when larvae were fed manure cattle
enriched with fish by-products, this content increased up to 4% (St-Hilaire et al.
2007a).
8 1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

Any change in the profile or the lipid composition of the diet directly affects the
lipid–volatile component, then the aroma and flavour of fish (Turchini et al. 2007),
and can therefore dramatically modify the perception of the product by the
consumer.
The inclusion of insect meals could thus influence the sensory properties of fish
products even if the information available, till now on this aspect, did not highlight
any negative effect. For instance, the results of a panel test (aroma and texture)
using fish (catfish and tilapia) fed chopped HI larvae alone or in combination with
commercial diets indicated that fish were scored and ranked similarly with regard to
control diets (Bondari and Sheppard 1981). In the same way, no significant dif-
ferences were detected by panellists comparing fish fed with diets containing HI
meals and fish fed with FM-based diets (Borgogno et al. 2017; Lock et al. 2016;
Sealey et al. 2011a). The influence of dietary inclusion of insect meals on fillet or
whole body composition (WBC) lead to controversial results. Some authors
reported decreased values of DM and ether extract (EE) with the inclusion of insect
meals (Belforti et al. 2015; Dong et al. 2013; Kroeckel et al. 2012; Ogunji et al.
2008a). Concerning crude protein (CP) content, only two trials reported changes
(Belforti et al. 2015; Ng et al. 2001) while others did not find any influence of insect
meal inclusion on this value (Gasco et al. 2016; Kroeckel et al. 2012; Ogunji et al.
2008a; Sealey et al. 2011a).
A problem often reported using insect meals in fish feeds is their high chitin
content. Chitin is a primary component of the insect exoskeletons and it is con-
sidered as poorly digestible by fish, due to a reduced enzyme activity (Gasco et al.
2016; Henry et al. 2015; Rust 2002; Sánchez-Muros et al. 2014). The presence of
chitinase, chitobiase and lysozyme has been reported in several species (Gasco et al.
2016; Henry et al. 2015). Nevertheless, because of the complex matrix in which
chitin is encompassed, the enzyme activity seems to be limited, reducing thus the
overall nutrient digestibility (Belforti et al. 2015; Henry et al. 2015; Sealey et al.
2011a).
Insect meals producers can reduce the content of chitin through extraction
process (Belluco et al. 2013; Sánchez-Muros et al. 2014) or its digestibility can be
increased through dietary enzyme inclusion (Henry et al. 2015) but these tech-
nologies are still not fully applied and studies need to be implemented. For instance,
the inclusion of exogenous enzymes (carbohydrases or proteases) in diets for
European sea bass did not improve the protein and fibre digestibility (Gasco et al.
2016).
It has to be underlined that low levels of chitin have been reported to have
immune stimulants (Esteban et al. 2001; Henry et al. 2015, 2018; Hoffman et al.
1997; Lin et al. 2012), bacteriostatic (Vidanarachchi et al. 2010) or antifungal and
antimicrobial properties (Faruck et al. 2016; Khoushab and Yamabhai 2010).
Insects also contain antimicrobial peptides that have been proved to be active
against Gram-positive and Gram-negative bacteria and to have antifungal proper-
ties. Great attention is then paid to their possible use as natural antibiotic or anti-
fungal (Yi et al. 2014; Żyłowska et al. 2011).
1.2 Insect Meals 9

Positive results on the fish immune status and resistance to diseases were
observed with the supplementation of 2.5% of MD meal in black carp
(Mylopharyngodon piceus) (Ming et al. 2013). Higher survival rates in fish fed with
insect meals have been reported when compared to fish with fed other protein
sources (Atse et al. 2014).
While several papers reported the possible negative effects of plant proteins on
histology of liver and gastrointestinal tract (Oliva-Teles et al. 2015), very few
information is available on the consequences of the dietary inclusion of insect
meals. First investigations on these aspects are promising with no statistical dif-
ferences detected for histology or morphometry parameters between fish fed with
insect diets and control diets (Lock et al. 2016; Renna et al. 2017).
Results on the use of insect in aquaculture species are dramatically impacted by
the type of used larvae, its condition (fresh or dried, whole, ground, defatted) or the
method of nutrient isolation and processing (sun drying, thermal treatments, lipid
extraction methodologies) and, of course, the fish species object of the
experimentation.
As far as whole or cut, live or frozen larvae are concerned, they were mainly
tested on warm water fishes and detailed results can be found in Henry and
coworkers (Henry et al. 2015).

1.2.1 Tenebrio Molitor

Several experiments have shown that TM meal could be used in partial or total
substitution of FM or other conventional protein sources. The level of TM meal
inclusion ranged from 8 to 50% substituting up to 100% of FM. Performances
results are unequal and bad performances are usually assigned to deficiency of some
nutrients when high levels of inclusion were performed. In African catfish finger-
lings, no significant differences were found up to 40% of FM substitution while a
significant reduction in all parameters was observed when 60% or more of the FM
component was replaced by TM (more than 26% of inclusion) (Ng et al. 2001).
Roncarati and coworkers performed a pre-fattening trial substituting 50% of FM in
common catfish (Ameiurus melas) fingerlings diets (Roncarati et al. 2015). Lower
final body weight was found in fish fed with TM diet compared to control diet
without TM even if results were still considered as acceptable.
Sánchez-Muros and coworkers investigated the nutritive value of a full-fat TM
larvae meal as partial protein replacement of FM and SBM in Nile tilapia
(Oreochromis niloticus) fingerlings (Sánchez-Muros et al. 2015). The dietary
inclusion up to 430 g/kg of TM meal worsened performance parameters.
Differences on feeding rate (FR), feed conversion rate (FCR), protein efficiency rate
(PER) and specific growth rate (SGR) were observed with diets containing
increasing levels of TM inclusion (Belforti et al. 2015). Recently, Gasco and col-
leagues evaluated the effects of dietary inclusion of a full-fat TM larvae meal on
European sea bass (Dicentrarchus labrax L.) juveniles (Gasco et al. 2016).
10 1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

Dietary TM inclusion level of 50% led to a worsening of final body weight, weight
gain (WG), SGR and FR. Piccolo and coworkers found that TM larvae meal can
replace FM up to 25% of inclusion in the diet for Sparus aurata without negative
effects on weight gain, CP and ether extract digestibility, and marketable indexes
after 163 days of feeding (Piccolo et al. 2017). On the contrary, when TM larvae
meal was included at 50%, nutrients digestibility and dressed yield were penalized.
Moreover in blackspot sea bream, the use of TM meal as an alternative dietary
protein source did not show detrimental effects on fish growth performance even if
its effects on fillet quality should be considered (Iaconisi et al. 2017).

1.2.2 Hermetia Illucens

Hermetia illucens larvae have been the subject of study for their exceptional ability
to grow on organic waste, giving a value of greater sustainability to the obtained
meal. As highlighted for TM, the meal preparation methods affect substantially the
trial results. In general, the replacement of FM meal with HI meal is higher when a
defatted meal is used.
On channel catfish (Ictalurus punctatus) decreased WG was observed using diets
containing 10% of HI meal inclusion (Bondari and Sheppard 1987) in cage culture,
while no statistical differences were reported (Newton et al. 2005) including up to
30% of HI prepupae meal in total FM and partial SBM substitution. Using dried
full-fat prepupae meal in rainbow trout diets, St-Hilaire and coworkers were able to
obtain inclusion levels of 15% without adverse effect on WG, feed intake (FI) and
FCR (St-Hilaire et al. 2007b). Moreover, this diet allowed a 38% reduction in FO
(i.e. from 13 to 8%). Highest levels of inclusion (30%) worsened all parameters.
Later, Sealey and coworkers evaluated the growth and sensory parameters of trout
fed diets having increasing levels (25 and 50%) of FM substituted with normal
(NHI) or fish offal-enriched black soldier fly (EHI) prepupae meal (Sealey et al.
2011a). Growth of fish fed with the EHI diets was not significantly different from
those fed with the FM-based control diet, while the growth of fish fed with the NHI
diets was significantly reduced. The fatty acid profile was influenced by dietary
treatments but fish fed with EHI highlighted good EPA and DHA contents. No
differences were highlighted in a blind sensory comparison of fish fed with the FM
control diet as compared to fish fed with the EHI or NHI diets.
On juvenile turbot (Psetta maxima), Kroeckel and coworkers tested partially
defatted HI prepupae meal and found a general worsening of performances at the
inclusion levels higher than 33% (Kroeckel et al. 2012). Moreover, authors found a
decrease of FI with increasing HI meal incorporation, due to low palatability. The
authors suggested that the presence of chitin might have influenced the FI, avail-
ability and digestibility of the nutrients and therefore growth performance.
Nevertheless, as HI was produced on local greenhouse waste streams, the authors
concluded that it could be a sustainable alternative protein source in partial sub-
stitution of FM (Kroeckel et al. 2012).
1.2 Insect Meals 11

In Atlantic salmon, the FM replacement by two different HI larvae meals,

varying in their protein and fat contents, led to controversial results (Lock et al.
2016).
A FM-based control diet and a vegetable protein-based diet were tested against
two HI larvae diets (18.5 and 37.5 of HI inclusion in substitution of 25 and 50% of
FM) for Siberian sturgeon (Acipenser baerii) juveniles (Gasco et al. 2017).
Preliminary results indicated that the inclusion of HI significantly affected fish
performances and condition factor. Generally, up to 25% of FM substitution, fish
performed as well as FM- and vegetable protein-based diets.
Results from a trial using a partially defatted HI larvae meal as potential feed
ingredient in rainbow trout diet showed that survival, growth performance, con-
dition factor, somatic indexes and dorsal fillet physical quality parameters were not
affected by diet (Renna et al. 2017). The use of HI larvae meal induced a decrease
of valuable polyunsaturated fatty acids (PUFA) in trout dorsal fillet even if the
differences were only reported at the highest level of HI inclusion. The HI worsened
the lipids health indexes of the same muscle.

1.2.3 Musca Domestica

In Africa, sustainable local production of insects is conceivable considering the

environmental conditions. Moreover, the rise of imported fish feed price has pushed
the research for more sustainable source of protein for several livestock production
systems, including fish (Makkar et al. 2014). Due to their ubiquitous nature and the
short time needed from eggs to suitable larvae for feed purposes, MD have been
extensively evaluated in fish diets, primarily with warm water fish species (Henry
et al. 2015).
Dietary inclusion levels performed ranged from 7.5 to 100%. Even if perfor-
mance results were not always positive, MD meals are considered to be sustainable
and economically interesting (Adewolu et al. 2010; Aniebo et al. 2009; Fasakin
et al. 2003; Makkar et al. 2014; Olele 2011; Sogbesan et al. 2006), as the cheapest
and more easily accessible for farmers. Moreover, often maggots are reared on
manure helping in the control of the nuisance dung (Sogbesan et al. 2006).
Results on fish are variable in relation to breeding conditions and larvae treat-
ment. In particular, Fasakin and coworkers evaluated drying and processing
methods (hydrolysed, defatted, full-fat, sun-dried and oven-dried maggots), on
growth and utilization of African catfish (Clarias gariepinus) diets highlighting
how these influenced the nutrient composition of obtained meal (Fasakin et al.
2003). The authors stated that fish performed better when fed with diets containing
defatted MD larvae meals than full-fat MD larvae meal. In diets for Clarias
gariepinus fingerlings, Idowu and coworkers substituted whole MD larvae meal to
FM and SBM without noticeable differences up to 25% of MD inclusion with 50%
of replacement (Idowu et al. 2003).
12 1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

Positive results in terms of growth performances have also been reported

(Sogbesan et al. 2006) in hybrid catfish diets, when the replacement of the FM
using oven-dried maggot meal reached 25% (dietary inclusion level of 7.5%).
A whole MD larvae meal (oven-dried) has also been studied in the diet of
rainbow trout but with little success, as an inclusion of 9.2% (25% of FM substi-
tution) resulted in a decrease of production parameters and to a deterioration in fish
quality (lipid FA profile) (St-Hilaire et al. 2007b).
The fish performance, the concentration of plasma glucose, the cortisol and
blood characteristics of Oreochromis niloticus fingerlings fed with increasing levels
of MD meal in diets were evaluated (Ogunji et al. 2008b). The inclusion of MD
larvae meal in the diet did not impair fish growth and performance. At the same
time, no adverse or stress effect on the haematology and homeostasis was observed.
Moreover, no significant difference was observed in liver glycogen reserve and in
hepatic catalase, activity did not differ significantly. The authors reported elevated
glutathione S-transferases activities when fish received higher dietary magmeal
concentration.
Adewolu and colleagues evaluated an animal protein mixture containing MD
larva meal in diets for Clarias gariepinus fingerlings (Adewolu et al. 2010). The
inclusion up to 50% of animal protein mixture did not influence the performances
parameters. However, in fish fed with highest FM substitution levels, these indi-
cators were significantly lower.
Dong and coworkers investigated the effect of dietary supplementation with MD
maggot meal or SBM on the growth performance and antioxidant responses of gibel
carp and dark barbel catfish (Dong et al. 2013). Interestingly, even if MD inclusion
lead to a worsening of some performances when compared to the control diet, fish
fed with MD diets exhibited equal or better results compared to fish fed with SBM
diets. Moreover, the MD supplementation enhanced the antioxidant capacity in
gibel carp. Positive results have also been reported (Ming et al. 2013) on the black
carp, where the replacement of the FP has reached 25%.
Feeding African catfish (Heterobranchus longifilis) larvae with
non-isonitrogenous nor isoenergetics diets containing different protein sources, Atse
and coworkers reported similar or better performances in fish fed with MD diets if
compared to fish fed with Artemia salina or fish by-products diets even if the CP
was lower (Atse et al. 2014). If compared to other protein sources based diets,
(blood, brain or SBM) MD always showed better results. When diets were fortified
with minerals, vitamins and amino acids premix, MD-fed fish reported the highest
performances. The survival rate was also always higher in fish fed with MD
compared to other groups.
Recently, Lin and colleagues reported that MD meal can be included up to 30%
without negative effects on growth and feed utilization of barramundi and no major
influence on body composition (Lin and Mui 2016). When oxidative status and
immune responses are considered, the inclusion rate of 10% corresponding to a FM
substitution of about 25% is recommended.
1.3 Poultry by-Product Meals 13

1.3 Poultry by-Product Meals

Poultry by-product meal (PBM) is a high protein source commonly used in

domestic animal feeds. The Association of American Feed Control Officials defines
PBM as the ‘ground, rendered, clean parts of the carcass of slaughtered poultry
such as necks, heads, feet, undeveloped eggs, gizzards and intestines (provided
their content is removed), exclusive of feathers (except in such amounts as might
occur unavoidably in good processing practices)’ (AAFCO 2010).
In recent years, mainly two PBMs are available in the market: feed grade and pet
food grade. The former, less expensive, is usually considered as produced from
low-quality by-product fractions and contains a higher level of ash and lower
protein content (Aldrich 2006; Dozier and Dale 2005). The latter, due to its high
price and quality, is mostly used in pet foods.
Poultry by-product meal quality and nutritional value (Tables 1.4 and 1.5) can
change from one batch to another depending on the included materials and on the
processing (time and temperature of the cooking process) applied for the production
(Cruz-Suárez et al. 2007; Dale et al. 1993).
As for all the rendering processes, the PBM production involves the application
of heat, the extraction of moisture and the separation of fat (Cruz-Suárez et al. 2007;
Meeker and Hamilton 2006). The applied rendering process enables the destruction
of pathogenic microorganisms and provided aseptic protein product free of potential
biohazards and environmental threats (Hamilton et al. 2006). Technological
developments in the production process have significantly improved the quality of
PBM (Badillo Zapata et al. 2016; Cruz-Suárez et al. 2007; Sealey et al. 2011b).
Nowadays, due to its high nutritional quality, large availability and palatability,
PBM has considerable potential as feed ingredient for aquaculture providing sub-
stantial feed cost saving (Hernández et al. 2010).
The PBM protein content ranges from 51.6 to 81 (% DM); despite a relatively
good amino acid profile, as far as fish nutrition is concerned, lysine and methionine
are often reported as the first limiting EAA (Castillo-Lopez et al. 2016; Hertrampf
and Piedad-Pascual 2000; Nengas et al. 1999; Rawles et al. 2006; Riche 2015;
Rossi and Davis 2012). Its average gross energy content is similar to the one shown
by insect meals and varies between 16 and 25 MJ/kg DM. The crude fibre content
is very low (about 1%) while the level of ash varies between 5 and 30%. As far as
fat content is concerned, publications reported values from 6.7 to 22.5%. PBM has
very low content in precious n-3 FA (EPA, DHA) (NRC 1993; Sealey et al. 2011b).
This can cause problems at high levels of inclusion, especially in juveniles or
marine species. Particular attention during the diet formulation and the inclusion of
appropriate quantities of FO in diets can overcome the problem but increase the
feed price (Sealey et al. 2011b).
As far as ADC of nutrients is concerned, the majority of the trials were carried
out with salmonids. The first one was that of Cho and Slinger who found quite low
CP digestibility (about 70%) in rainbow trout (Cho and Slinger 1979). Research
performed over the successive years showed different results (Bureau et al. 1999;
14 1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

Table 1.4 Nutrient composition and nutritive value of poultry by-product meal (PBM) compared
to fishmeal (FM) and soybean meal (SBM). Values are reported as mean of values found in the
cited references (with minimum and maximum values). The following chemical data are shown
here: dry matter (DM), crude protein and essential amino acids, ether extract and fibre
Unit PBMa FMb SBMc
Dry Matter (DM) % as fed 93.7 (82.4–97.4) 92.1 (90.0–94.4) 87.9 (85.0–92.1)
Crude protein % DM 66.1 (51.6–81.0) 75.6 (70.2–80.7) 51.4 (48.3–54.5)
Lysine % protein 4.4 (3.3–8.2) 6.1 (5.5–7.5) 6.1 (5.7–6.6)
Methionine % protein 1.4 (1.0–2.0) 2.2 (2.0–2.6) 1.4 (1.2–1.6)
Methionine + Cystine % protein – 2.9 (2.6–3.2) 2.9 (2.5–3.3)
Tryptophan % protein 0.5 (0–0.8) 0.8 (0.7–0.9) 1.3 (1.2–1.4)
Threonine % protein 2.8 (1.9–3.9) 3.1 (2.9–4.3) 3.9 (3.5–4.3)
Leucine % protein 5.0 (3.9–9.7) 5.9 (5.2–7.3) 7.5 (6.8–8.0)
Isoleucine % protein 2.7 (1.8–4.7) 3.7 (3.3–4.4) 4.6 (4.3–5.0)
Valine % protein 3.1 (2.2–5.2) 4.2 (3.9–4.8) 4.8 (4.3–5.4)
Histidine % protein 1.9 (1.2–5.6) 1.8 (1.7–1.9) 2.6 (2.4–2.9)
Arginine % protein 5.1 (3.2–8.8) 4.6 (4.0–6.0) 7.4 (6.8–8.1)
Phenylalanine % protein 2.8 (2.2–4.0) 5.5 (5.2–6.5) 8.5 (7.7–9.4)
Ether extract % DM 13.8 (6.7–22.5) 8.1 (2.0–12.0) 2.1 (2.0–2.2)
Crude fibre % DM 1.1 (0.5–2.1) – 6.7 (3.5–10.1)
a
Data from: Barreto-Curiel et al. (2016), Bureau et al. (1999), Castillo-Lopez et al. (2016), Cheng
and Hardy (2002), Cruz-Suárez et al. (2007), de Carvalho et al. (2016), Dozier and Dale (2005),
El-Haroun et al. (2009), Fasakin et al. (2005), Feedpedia: http://www.feedipedia.org, Goda et al.
(2007), Guimarães et al. (2008), Hernandez et al. (2010), Hernandez et al. (2014), Li et al. (2009),
Ma and Wang (2014), Nengas et al. (1999), Riche (2015), Sealey et al. (2011b), Shapawi et al
(2007), Subhadra et al. (2006), Sugiura et al. (1998), Wang et al. (2006), Wang et al. (2016), Yang
et al. (2004)
b
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
c
Data from: Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)

Cheng and Hardy 2002; Dong et al. 1993; Guimarães et al. 2008; Hernández et al.
2010; Pfeffer et al. 1995; Sugiura et al. 1998). The ADC improvement obtained
over the years reflects the improvement of PBM processing methodologies, but also
supported the hypothesis that nutrients ADC is highly dependent on the PBM
origin, quality and the faecal collection methodology.
Several researches have shown the high potential of PBM in aquaculture feeds.
The dietary inclusion level, as well as the FM or other conventional protein sources
substitution, varies among fish species mainly due to the PBM quality and the diet
formulation. Reduced performances with high levels of FM substitution are often
associated with decreased protein digestibility or deficit in EAA or essential FA
(Badillo Zapata et al. 2016; Gaylord and Rawles 2005; Parés-Sierra et al. 2014;
Shapawi et al. 2007). Furthermore, increased attention has recently been paid to the
lower taurine content of PBM compared to FM. Historically, taurine has not been
considered as an EAA (El-Sayed 2014; Salze and Davis 2015). Nevertheless,
recently it has been demonstrated that the ability to synthesize taurine widely varies
1.3 Poultry by-Product Meals 15

Table 1.5 Nutrient composition and nutritive value of poultry by-product meal (PBM) compared
to fishmeal (FM) and soybean meal (SBM). Values are reported as mean of values found in the
cited references (with minimum and maximum values). The following data are shown here:
minerals (ash), calcium, phosphorus, sodium, potassium and gross energy
Unit PBMa FMb SBMc
Minerals (ash) % DM 15.0 (5.1–29.7) 16.6 (12.0–23.3) 6.9 (6.8–7.0)
Calcium % DM 5.1 (2.2–9.9) 36.3 (15.4–78.3) 3.9 (2.3–6.3)
Phosphorus % DM 2.7 (1.6–5.0) 25.9 (19.0–40.4) 6.9 (5.8–8.6)
Sodium % DM 0.6 (0.5–1.0) 10.0 (5.9–14.4) 0.1 (0.0–0.8)
Potassium % DM 0.8 (0.4–1.8) 10.2 (5.9–14.4) 23.7(21.8–26.0)
Gross energy MJ/kg DM 21.2 (16.2–24.9) 21.4 (19.6–23.8) 19.9 (19.8–20.0)
a
Data from: Barreto-Curiel et al. (2016), Bureau et al. (1999), Castillo-Lopez et al. (2016), Cheng
and Hardy (2002), Cruz-Suárez et al. (2007), de Carvalho et al. (2016), Dozier and Dale (2005),
El-Haroun et al. (2009), Fasakin et al. (2005), Feedpedia: http://www.feedipedia.org; Goda et al.
(2007), Guimarães et al. (2008), Hernandez et al. (2010), Hernandez et al. (2014), Li et al. (2009),
Ma and Wang (2014), Nengas et al. (1999), Riche (2015), Sealey et al. (2011b), Shapawi et al
(2007), Subhadra et al. (2006), Sugiura et al. (1998), Wang et al. (2006), Wang et al. (2015), Wang
et al. (2016), Yang et al. (2004)
b
Data from Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)
c
Data from Feedpedia: http://www.feedipedia.org, Guillame et al. (2001)

among fish species because of the different activities of key enzymes in its
biosynthesis pathway (El-Sayed 2014; Rossi and Davis 2012; Salze and Davis
2015).
High levels of FM replacement could lead to decrease the taurine content beyond
a limit level causing decrease in performances (Rossi and Davis 2012). The dietary
supplementation with taurine could allow highest levels of FM substitution, in
particular, when plant-based proteins are also present in the diets formulation
(Chatzifotis et al. 2008; Rossi and Davis 2012; Salze and Davis 2015).
The minimum level of FM needed in fish fed with PMB to support good per-
formances is species dependent (Table 1.6). Rossi and Davis showed that 5% of
FM is sufficient in Florida pompano when 15% of PBM is used (Rossi and Davis
2012). Compared to a control diet containing 35% FM, 10% of PBM, 15% of SBM
and 10% of rapeseed meal, Ma and Wang found reduced performances already at
40% of FM substitution (further 15% of PMB dietary addition) in a trial performed
with Golden pompano (Trachinotus ovatus) juveniles suggesting that levels higher
than 21% of FM are needed (Ma and Wang 2014). Using a locally produced PBM
(29.2% of inclusion), Nengas and colleagues reduced the level of FM up to 35% in
Sparus aurata diets with slight (but not statistical) performances reduction (Nengas
et al. 1999). Lower levels of FM requirements were found for Japanese sea bass
(8%) (Wang et al. 2015), red drum (10%) (Kureshy et al. 2000), Malabar grouper
(25% and 13% reported by Wang and coworkers and Li and colleagues, respec-
tively, Li et al. 2009; Wang et al. 2008), and cuneate drum (18%) (Wang et al.
2006). Badillo-Zapata and colleagues found that the total replacement of FM with
PBM in diets for Totoaba macdonaldi juveniles led to worsened performances and
Table 1.6 Maximum level of FM substitution (and PBM inclusion) with PBM reached without impairing any of the performance parameter evaluated
16

Fish Species Max level of % PBM % FM in Other CP and CL Observation Reference

FM inclusion control protein diet content
substitution diet source
Sparus aurata 50 29.2 72.9 – 45–13 Locally produced PBM Nengas et al.
(1999)
Morone chrysops x 100 30 30 SBM 40–6 Decreased (but not statistically different) Webster et al.
M. sexatilis (30) performances (2000)
Carassius auratus 15 10.8 46.3 – Yang et al.
gibelio (2004)
Oreochromus 66 30.3 44 – Best productivity values (WG, FCR, SGR, Fasakin et al.
niloticus x O. PER) but not statistical differences vs FM diet (2005)
mossambicus
Scophthalmus 25 21.2 77.3 – 55–15 Turker et al.
maeoticus (2005)
M. chrysops x M. 35 17.2 25 PBM 42.5–11 Further 9.47% PBM inclusion Rawles et al.
sexatilis (7.73) (2006)
SBM
(25.9)
D. labrax 50 17.5 35 BM (3) 42.5–12.5 Wang et al.
(2006)
Carassius auratus 100 53 53 – 38–9.5 The optimal replacement level of FM by PBM Yang et al.
gibelio was estimated by second-order polynomial (2006)
regression to be 66.5% in protein
Psetta maeotica 50 43.2 77.3 – Yigit et al.
(2006)
Clarias gariepinus 100 34.5 25 – 25.5–8.5 Trial performed comparing also other protein Goda et al.
sources as FM substitute (2007)
Cromileptes 50 and 100 36.1 and 69.4 – Pet food grade PBM enable 100% FM Shapawi et al.
altivelis 74 replacement while feed-graded PBM allowed (2007)
1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

only 50% replacement

(continued)
Table 1.6 (continued)
Fish Species Max level of % PBM % FM in Other CP and CL Observation Reference
FM inclusion control protein diet content
substitution diet source
Epinephelus 50 11.5 50 – 53–9 Wang et al.
malabaricus (2008)
Oncorhynchus 30 30 40 CGM 49–23.5 PBM partially replaced FM and CGM (total El-Haroun
mykiss (28) replacement of BM) et al. (2009)
BM (6–
1.3 Poultry by-Product Meals

12)
Epinephelus 50 22.8 50 BM 53–9.6 Fish fed with the 75% PBM diet had a Li et al. (2009)
malabaricus (5.7) significantly lower FI than fish fed with FM or
25% PBM diets
O. niloticus 100 26.5 27 SBM 35.5–6.8 High quality PBM Hernández
(12) et al. (2010)
CGM (9)
O. mykiss 100 63.8 68.6 – 48.3–18.7 High quality PBM Sealey et al.
(2011b)
Rachycentron 60 30 50 SBM 45–11 Improved PER and FER in fish fed with 15 and Zhou et al.
canadum (11.3) 22.65 PBM inclusion. A quadratic regression (2011)
indicated at 30.75% FM the optimal
replacement level for PER value.
Trochinotus 67 9.8 15 SBM 40–8 Fish growth performance reduced when FM Rossi and
carolinus (50) was completely removed from the diets. Davis (2012)
Oncorhynchus 100 59 66 – 43–12.5 Fish fed with the 67% PBM diet had a Badillo et al.
mykiss significantly higher FBW than the rest of the (2014)
treatments, whereas the 100% PBM had a
significantly lower FBW than 67% PBM
Lutjanus guttatus 65 39.4 52.6 SQ (6) 51.5–16 Fish fed with Hernández
K (7.6) the 87% PBM showed worsened (not always et al. (2014)
17

stat. different) values

(continued)
Table 1.6 (continued)
18

Fish Species Max level of % PBM % FM in Other CP and CL Observation Reference

FM inclusion control protein diet content
substitution diet source
O. mykiss 73.5 44 66 – 43.5–12.5 Parés-Sierra
et al. (2014)
Trochinotus 67 from 32.6 – 48.5–21 Five different types of PBM. FI reduced only Riche (2015)
carolinus 19.8 to with CC66 PBM type
22.3
Lateolabrax 80 38.7 40 SBM 47.5–11.5 Improved performances up to 80 substitution vs Wang et al.
japonicus (20) FM diets (2015)
RSM (8)
O. niloticus 100 26 20 SBM 30.2–11.5 Yones and
(15) Mewalli (2015)
CGM
(11)
Totoaba 67 45 65 – 51–8 Badillo-Zapata
macdonaldi et al. (2016)
Dicentrarchus 60 18.94 47.4 SBM 48–14 Srour et al.
labrax (11) (2016)
CG (11)
FM: fishmeal; PBM: Poultry by-product meal; CGM: Corn gluten meal
FM: Fishmeal; PBM: Poultry by-product meal; CGM: corn gluten meal; BM: blood meal; SQ: Squid meal; K: Krill meal; RSM: Rapessed meal; CG: Corn
gelatin
WG: Weight gain; FI: Feed intake; FR: feeding rate; PER: Protein efficiency ratio; FCR: Feed conversion ratio; IBW: Initial body weight (g); FBW: Final body
weight (g); FER: Feed efficiency ratio
CP: crude protein; CL: crude lipid
1 Fishmeal Alternative Protein Sources for Aquaculture Feeds
1.3 Poultry by-Product Meals 19

increased mortality and that PBM can be used in up to maximum 67% FM

replacement (Badillo-Zapata et al. 2016).
Wang and coworkers obtained 80% of FM replacement with diets containing
also other protein sources (SBM, rapeseed meal) showing a high capacity of
Lateolabrax japonicus in utilizing PBP nutrients (Wang et al. 2015). Recently, it
was theorized that low performances obtained with high levels of FM substitution
by PBM could be due to Selenium deficiency as the content of this essential nutrient
is lower in PBM than in FM (Wang et al. 2016). Webster and colleagues indicated
that diets without FM can be fed to juveniles sunshine bass without major negative
effects on performances (Webster et al. 2000). Similarly, Sealey and coworkers,
using a high-quality PBM, were able to substitute completely FM in rainbow trout
diets (Sealey et al. 2011b). In addition, Barreto-Curiel and colleagues positively
replaced 100% of FM in rainbow trout using a PBM mixed with acid fish silage
(Barreto-Curiel et al. 2016).
As far as WBC is concerned, modifications can occur when alternative protein
meals are used as FM replacers (Gatlin et al. 2007). The major effects of PBM
inclusion on WBC have been reported for the CP and crude lipid content. Goda and
colleagues found a reduction of the CP content in fish fed with 100% PBM as FM
replacer and these results were supported by the findings of Zhou and coworkers
(Goda et al. 2007; Zhou et al. 2011). Conversely, slightly higher CP values were
found in fish fed with PBM than those fed with FM-based control diet (Shapawi
et al. 2007; Yang et al. 2006). An increase of crude lipid WBC content was reported
in rainbow (Alexis et al. 1985; Steffens 1994), in European eel (Gallagher and
Degani 1988), in chinook salmon (Fowler 1991), in gilthead seabream (Nengas
et al. 1999), in Nile tilapia fingerlings (Hernandez et al. 2010) and in spotted rose
snapper (Hernandez et al. 2014).
The whole body fat increases in fish fed with diets having PBM were often
justified by high fat content in PBM. Nevertheless, several research reported no
differences in WBC even at high levels of PBM inclusion (El-Haroun et al. 2009;
Ma and Wang 2014; Riche 2015; Yones and Metwalli 2015). These contradictory
results support the theory that differences in utilization and transformation capacity
for PBM exist among fish species, and are related to the quality and quantity of
PBM used in diets formulation.
PBM has been widely studied and the improvement of quality due to better
processing technologies allows high levels of FM replacement. This may allow
reduction of feed cost formulation and increase in profitability. Nevertheless, as the
technological process of PAP production was revised (EC No. 94/449; temperature
over 133 °C, pressure, 3 bar by steam for 20 min; maximum particle size, 50 mm),
this could compromise nutritional quality and modify the reference values obtained
so far. Therefore, it is necessary to further evaluate these ingredients and research is
highly needed (Moutinho et al. 2017).
20 1 Fishmeal Alternative Protein Sources for Aquaculture Feeds

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