Future Foods 7 (2023) 100240

Contents lists available at ScienceDirect

Future Foods
journal homepage: www.elsevier.com/locate/fufo

Valorisation of industrial food waste into sustainable aquaculture feeds

Kaarunya Sampathkumar a,1, Hong Yu a,1, Say Chye Joachim Loo a,b,c,∗
a
School of Material Science and Engineering, Nanyang Technological University, 50 Nanyang Avenue, 639798 Singapore
b
Singapore Centre for Environmental Life Sciences Engineering (SCELSE), Nanyang Technological University, 60 Nanyang Drive, 67551 Singapore
c
Lee Kong Chian School of Medicine, Nanyang Technological University, 11 Mandalay Road, 308232 Singapore

a r t i c l e i n f o a b s t r a c t

Keywords: The increasing global population has put enormous stresses on food security. Aquaculture is a major source of
Food waste food fish and is considered one of the key pillars of our global food supply. The increasing aquaculture production
Agriculture has led to a surge in demand for fishmeal and fish oil – key ingredients of fish feeds obtained from finite marine
Sustainability
resources. Decreasing the dependence on marine resources could improve the sustainability of farmed fishes. One
Insect meal
strategy is to replace fishmeal with alternative proteins. This review aims to provide a comprehensive overview
Encapsulation
Fishmeal of how industrial food wastes can be valorised into a sustainable protein source as a replacement for fishmeal.
The direct substitution of fishmeal with food wastes and the challenges associated with it will first be discussed.
Next, a section will be devoted to repurposing of industrial food waste as insect feeds for the bioconversion of
waste into high value protein source. A special mention on the use of encapsulated micronutrients and probiotics
for functionalised feeds will also be reviewed. The review concludes by summarizing the existing regulations
on the use of waste in aquaculture, its public perception, and future perspectives in converting food waste into
aquaculture feed for a sustainable circular economy.

1. Introduction
The global population has been steadily increasing and the demand
for food is higher than what could be met by conventional farming meth-
ods. In fact, global food demand is expected to increase between 35% to
56% by 2050 (van Dijk et al. 2021). Hence, the current focus is to sta-
bilize food production and improve food security via sustainable ways,
so as to prolong existing resources for future generations.
Food fish is considered to be one of the highest sources of protein
in our diet, and global production of fish has quadrupled over the past
50 years (Hannah et al., 2021). In terms of fish consumption, it has
risen from 9.0 kg per capita in 1961 to 20.3 kg per capita in 2017. This
constitutes about 20% of the global average animal protein intake per
capita (Junning 2021). Overfishing has unfortunately reduced our sup-
ply from the sea, which also impacts the marine food chain (FAO 2022).
With an increasing demand for food fish, along with a depleting supply
of marine-harvested fish, food fish industries are now shifting their focus
on aquaculture production, with 82.1 million tonnes of aquatic animals
produced in 2018 (FAO 2021). Even with farmed fish, fish feed is the ma-
jor determinant of its production capacity and quality (Verdegem et al.,
2021). With the protein content ranging anywhere between 25 and
50% depending on the type of fish, the cost of aquaculture production
depends heavily on the protein source (Alfiko et al., 2022). The chal-
lenge in aquaculture is therefore to seek cost-effective alternative pro-
tein for aquafeeds from other sustainable sources. Some possible alterna-
tive protein sources have previously been reviewed (Kaushik and Hemre
2008; Gasco et al., 2018; Hua et al., 2019).
There have been increasing interests in recycling wastes gener-
ated from food processing, as a substitute for fishmeal in aquaculture
(Ma et al., 2019; Nasr et al., 2021). Industrial food waste, in the con-
text of this paper, refers to waste derived from the processing of plant-
based materials to obtain an edible product for human consumption.
Some examples include, soybean meal, sunflower oil meal, canola oil
meal, brewer’s spent grain etc. Each day a colossal amount of protein-
rich material generated from the food processing industry is discarded
as wastes, eventually occupying landfills or are incinerated (Li et al.,
2013b). For instance in 2019, 14 million tonnes of soybean processing
waste were generated globally (Privatti and Rodrigues 2021), giving
an indication of the magnitude, industrial food waste can impact the
economy. Incineration is one of the widely used methods for managing
non-recyclable waste, especially in land scarce countries. This can fur-
ther implicate the environment through the generation of greenhouse
gasses. utilizing food-derived protein-rich waste for aquaculture feeds
is thus a sensible solution to recycle the waste via a circular economy.

∗
Corresponding author.
E-mail address: joachimloo@ntu.edu.sg (S.C.J. Loo).
1
Equal contribution and first authorship.

https://doi.org/10.1016/j.fufo.2023.100240
Received 5 April 2023; Received in revised form 29 May 2023; Accepted 2 June 2023
2666-8335/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)
K. Sampathkumar, H. Yu and S.C.J. Loo Future Foods 7 (2023) 100240

Insect farming which involves feeding insects with waste, is another palm kernel meal, etc. These oilseed cakes or meals have shown a po-
strategy that is gathering interest of late. Insect bioconversion mitigates tency as animal feeds considering their nutritional values post process-
the disadvantages of feeding food waste directly to fishes and improves ing, specifically a high protein content (FátimaArrutia et al., 2020).
the nutritional profile of feeds (Sánchez et al., 2021; Rumpold and
Schlüter 2013). Aside from the nutritional value of insect meals, another
merit is its environmental friendliness (van Huis and Oonincx 2017).
2.1.1. Sunflower meal
Unlike other livestock, cultivation of insects usually does not require
Sunflower (Helianthus annuus L.) meal (SFM), which is a by-product
large spaces. Insects could be raised at a higher density in constrained
from sunflower oil extraction, with an estimated 21.85 million tons pro-
spaces that generates less greenhouse gasses. Furthermore, insects re-
duced globally in 2019 (Heuzé et al., 2019). Such massive waste pro-
quire much less food and water and are highly reproductive compared
duction has led to extensive studies in utilizing it as a fishmeal replace-
to livestock (Sánchez-Muros et al., 2014; Rumpold and Schlüter 2013;
ment. SFM could be an ideal plant-based protein given its high pro-
Salomone et al., 2017). Most importantly, insects are omnivorous and
tein levels – 27.8% to 37.4% of crude protein (Table 1) (Hassaan et al.,
they could feed on a wide-range of diets including industrial food wastes
2018). Furthermore, SFM is free of trypsin inhibitors and abundant in
(Rumpold and Schlüter 2013), thus being a sustainable approach.
vitamins compared to other plant-based proteins (Heuzé et al., 2019;
This review therefore aims to provide an overview of how food
Hertrampf and Piedad-Pascual 2000). Partial fishmeal replacement stud-
wastes can be valorised into protein meal in aquaculture feeds with
ies with high protein SFM (at just 12.5%) showed that Arctic charr at
the goal of replacing unsustainable fishmeal proteins. The first part of
the grow-out stage had similar final weight gain compared to conven-
the review explores the different sources of alternative protein gener-
tional fish feed. There was also no indication of gastrointestinal inflam-
ated as waste from the food processing industry, that can potentially be
mation (Smith et al., 2018a). Elesho et al. investigated digestibility of
exploited for aquaculture feeds. Detailed discussions on the challenges
fish feeds with different protein sources on African catfish. Inclusion
involved and the various strategies to overcome them are included.
of SFM (30%) could meet growth requirement for methionine – an es-
A dedicated section on the upcycling of plant proteins into fish feed
sential amino acid (Elesho et al., 2021). In combination with soybean
through insects will be discussed subsequently. A special mention on
meal, SFM was used as a fishmeal substitute on Clarias gariepinus. No
the use of encapsulation systems to incorporate functional ingredients
significant difference was observed in aspects of weight gain and crude
such as probiotics or amino acids for better performance of the feeds, is
protein level in fish after feeding trials compared to fishmeal based con-
also included. The paper concludes by providing a future perspective of
trols, and complete replacement with a combined plant-based protein
transitioning from fishmeal to other alternative proteins, along with the
diet exhibited improved feed conversion ratio (FCR) (Nasr et al., 2021).
changing policies and public perception of fish developed through waste
valorisation. This will provide an outlook on the future of industrial food
waste-based feed, in meeting to an increasing global food demand.
2.1.2. Sesame oil meal
Like SFM, sesame oil meal (SOM) is also a high nutritional value
2. Pristine food waste as protein substituent in fish feed (Direct
industrial food waste. Besides consuming it as food, sesame (Sesamum
substitution)
indicum) is usually cultivated for its oil. The solid residue part obtained
after the mechanical extraction of oil from seeds is SOM or sesame
Wastes generated from food industry ranges from conventional by-
oil cake. Sesame is cultivated world-wide, predominantly distributed
products of crops, processing waste from food industry, both plant
in Asia and Africa, with production as high as 4 million tons in year
and animal based, to industrial processing by-products of marine al-
2012 (Olude et al., 2016; Nang Thu et al., 2011). The global production
gae/macroalgae. Macroalgae or seaweed, is a protein rich product, with
amount was further increased to 5.5 million tons in year 2014, while
nearly 36 million tons (wet weight) produced globally in the year 2019
65% of harvested sesame seed was sent for sesame oil production, leav-
(Junning 2021). Of this, 90% was used for direct human consump-
ing a tremendous amount of SOM generated as waste (Heuzé; et al. 2021;
tion (Wei et al., 2013) and the rest 10% was used for carbohydrates
El-Beltagi et al., 2022). SOM is reported to have 420 g/kg, or a range
extraction by cosmetic or pharmaceutical industries (Bulota and Bud-
between 23% – 46% protein with high protein quality (Table 1) and low
tova 2016; Pardilho et al., 2022). Considering the comparatively small
crude fiber content (Nang Thu et al., 2011, Omer et al., 2019).
amount of processing waste being generated, macroalgae by-product
Direct addition of SOM into fish feeds as fishmeal alternative have
will not be discussed herein. As for animal processing by-products, they
been investigated. Das et al. attempted to fabricate floating fish feeds out
are produced from the processing of livestock, fishes, or poultries in
of SOM and compared these to commercial floating feeds. SOM based
food industries. During the processing, a substantial amount of animal
floating feeds exhibited similar weight gain and feed intake (FI) value
parts would be discarded as wastes (Martínez-Alvarez et al., 2015). It
for Labeo rohita. Furthermore, FCR was also improved when employing
has been reported that around 24 million tons of animal processing
SOM based floatable feed (Swain et al., 2021). One benefit brought by
by-products are generated every year from food industries (Martínez-
SOM is its palatability to fish. In a study of using SOM as fishmeal al-
Alvarez et al., 2015). As an animal-based protein source, animal process-
ternative in rainbow trout, SOM based feeds led to a higher growth rate
ing by-products could be included into animal feeds in both raw and hy-
for fish fry. This was attributed to a significantly improved voluntary in-
drolyzed forms, with less concerns of bringing adverse effects on growth.
take of these feeds (Nang Thu et al., 2011). The study also pointed out
Compared to plant-based industrial food wastes, animal processing by-
that SOM could replace 50% fishmeal in fish feeds for carnivorous fish
products are more complete in nutritional values, and are already being
without compromising the growth performance of fry (Nang Thu et al.,
used in aquafeeds (Zou et al., 2021; Bethi et al., 2021). Therefore, plant-
2011). The study by Guo et al. revealed that SOM incorporated diet for
based protein sources from industrial food wastes would be the focus
tilapia at juvenile state would not adversely affect survival rate, FCR,
of the review. The sources of industrial food wastes that are suitable
fish body dry matter, crude protein content, etc. There was also no liver
for fishmeal replacement can be segregated into two categories: oilseed
composition differences between SOM fed fish and control group indi-
cakes/meals and by-products from industrial food processing.
cating that inclusion of SOM into fish diets would not adversely affect
their growth (Guo et al., 2011). In a feeding trial (40% SOM) on Labeo
2.1. Oilseed cakes/meals rohita, no obvious difference in nutrient (i.e., protein, lipid) digestibil-
ity of fingerlings was observed (Roy et al., 2013). These studies indicate
Oilseed cakes or oilseed meals are solid residues from edible oil pro- SOM to be a promising plant-based protein source for fishmeal substi-
duction, such as sunflower meal, rapeseed meal, sesame oil meal or cake, tution.

2
 K. Sampathkumar, H. Yu and S.C.J. Loo
Table 1
Protein content of different industrial food wastes and possible adverse effects on aquaculture.

Industrial Protein content Fish species Optimal replacement Optimal FCR / FE Challenges Adverse effects towards fish (higher than References
food (%) (%) optimal inclusion level)
wastes

SFM 27.8% - 37.4% Arctic charr 12.5% 0.98 (FE, gain/feed) ANFs (fiber and phenolic Lower digestibility (Smith et al., 2018b; Elesho et al., 2021;
African catfish 30% - compounds) Higher FCR Nasr et al., 2021; Heuzé et al., 2019;
Clarias gariepinus 100% (combination 1.90 (FCR) sulfur amino acids Lower SGR Hassaan et al., 2018; Hertrampf and
with SBM) deficiency Piedad-Pascual 2000; Olvera-Novoa et al.,
2002)
RM 32% - 45% Pseudobagrus ussuriensis 10% 66.15 (FE,%) ANFs (fiber and phytic Lower SGR, FE and protein efficiency ratio (Bu et al., 2018; Xu et al., 2019;
Gibel carp 100% (not 45.53 (FE,%) acid) Hernández et al., 2013; Hertrampf and
Rainbow trout optimization study) 63.60 (FE,%) Deficient in lysicne and Piedad-Pascual 2000; Plaipetch and
10% methionine Yakupitiyage 2013; Shafaeipour et al.,
2008; Xu et al., 2019)
SOM 420 g/kg Labeo rohita 20% 1.94 (FCR) Lysine deficiency Lower growth rate, weight gain and SGR (Nang Thu et al., 2011; Omer et al., 2019;
23% - 46% Rainbow trout 50% 1.08 (FE, gain/feed) ANFs (phytate) Higher FCR Swain et al., 2021; Guo et al., 2011;
Nile tilapia 16% (combination 1.23 (FCR) Roy et al., 2013; Hasan et al., 1997;
with SBM) Mohanta et al., 2007)
PKM 20% - 25% Nile tilapia 30% 1.05 (FCR) ANFs (crude fiber) Lower growth rate (Hertrampf and Piedad-Pascual 2000;
15% - 18% Tambaqui 25% 1.24 (tank conditions) / Low protein content Higher FCR Heuzé et al., 2016; Omoregie and
3

1.02 (field conditions) Lower protein retention efficiency Ogbemudia 1993; Obirikorang et al.,
(FCR) 2015b) (Omoregie and Ogbemudia 1993;
Yinhui et al., 2004; Silva et al., 2020;
Obirikorang et al., 2015a)
SBM 16.1% - 33.4% Nibea miichthioides 20% 1.14 (FCR) ANFs (protease, trypsin Poor palatability (Li et al., 2013a; Li et al., 2012;
Nile tilapia 75% - inhibitor, phytates, etc.) Gastrointestinal inflammation Wang et al., 2006; Goda et al., 2007;
Channel catfish 100% - Methionine and cystine Lower weight gain, survival rate Wang et al., 2017; Matulic et al., 2020;
African catfish 100% 2.94 (FCR) deficiency Higher FCR Ma et al., 2019; Hertrampf and
Orange-spotted grouper 50% 0.84 (FE, gain/feed) Piedad-Pascual 2000; Huynh and
Ameiurus nebulosus L. 50% 1.49 (FCR) Nugegoda 2011; Ajani et al., 2016)
BSG 15% - 24% Rainbow trout 30% 1.37 (combination with ANFs (fiber) Impairment of apparent digestibility (Mussatto 2014; Nazzaro et al., 2021;
Gilthead seabream 30% BSY) (FCR) Lysine, methionine and coefficient Jayant et al., 2018; Hertrampf and
Pangasianodon hypophthalmus 50% 2.03 (combination with cystine defficiency Piedad-Pascual 2000; Fernandes et al.,
BSY) (FCR) 2022; He et al., 2020; Naylor et al., 2009)
1.65 (combination with
SBM) (FCR)
BSY 40% - 50% Pangasianodon hypophthalmus 45% 2.40 (FCR) Cell wall of yeast Affect nitrogen digestibility (Marson et al., 2020; Pongpet et al., 2016;
x Pangasius bocourti 30% 1.28 (FCR) Bitter taste Poor palatability Oliva-Teles and ̧alves 2001; Nguyen et al.,
Seabass 40% 4.32 (FCR) 2019; Hertrampf and Piedad-Pascual
Giant freshwater prawn 2000; Ferreira et al., 2010)
SFM – Sunflower Meal; RM – Rapeseed Meal; SOM – Sesame Oil Meal; PKM – Palm Kernel Meal; SBM – Soybean Meal; BSG – Brewer’s Spent Grain; BSY – Brewer’s Spent Yeast; FCR – Feed Conversion Ratio; FE –

Future Foods 7 (2023) 100240

Feeding Efficiency; ANF – Antinutritional Factor; SGR – Specific Growth Rate.
K. Sampathkumar, H. Yu and S.C.J. Loo
2.1.3. Rapeseed meal
Rapeseed (Brassica napus) meal (RM), also called canola meal, is usu-
ally obtained from rapeseed or canola oil production. By year 2018,
worldwide production of RM reached 38.8 million tons (Heuzé et al.,
2020). In aquaculture, RM is one of the important plant-based protein
sources with protein content in the range of 32% to 45% (Table 1)
(Bu et al., 2018). When 10% to 20% fishmeal was substituted with RM,
Pseudobagrus ussuriensis could maintain comparable weight gain and sur-
vival rate, and this inclusion of RM into fish feeds did not adversely
affect crude protein level and muscle composition of fish (Bu et al.,
2018). This implied that RM protein could be effectively and efficiently
digested by Pseudobagrus ussuriensis for their growth and body construc-
tion within the substitution percentage mentioned in the study. Signifi-
cant evidence of interactions between fish strain and feeding diets were
observed by Xu et al. where Gibel carp strain Dongting (DT) showed the
highest FI towards RM diet compared to other diets (i.e., fishmeal and
soybean meal) (Xu et al., 2019). According to their analysis, the geno-
type of fish and diet interaction could greatly influence feed intake. Two
genes, srebp1 and fas, were involved in improved FI for Gibel carp strain
DT. srebp1 is responsible for lipid synthetic transcriptional factor while
fas regulate lipogenic process. The higher transcriptional level of both
genes in strain DT contributed to higher FI of fish fed with RM (Xu et al.,
2019). Similar results were also observed for rainbow trout fed with fish
feed incorporated with 10% RM, where survival rate, weight gain and
FI were comparable to the control group (Hernández et al., 2013).
2.1.4. Palm kernel meal
As a by-product from palm oil production, palm kernel meal (PKM) is
mostly generated in Southeast Asia (i.e., Indonesia, Malaysia) with mil-
lions tons of annual production (Heuzé et al., 2016). Though PKM may
not have comparable protein content as other oilseed meals (Table 1),
its protein is considered of high quality (Omoregie and Ogbemudia
1993), with no toxicity reported when used in aquaculture (Yinhui et al.,
2004). Application of PKM in fish feeds has been investigated consider-
ing its potential as a protein or energy source (Silva et al., 2020). For
instance, in a study on the effects of different PKM inclusion percentage
on tilapia growth performance, 15% inclusion of PKM as fishmeal al-
ternative showed the best performance with higher specific growth rate
(SGR) and lower FCR value (0.74 and 0.86, respectively) (Omoregie and
Ogbemudia 1993). It was also reported that a maximum of 30% in-
clusion would not compromise dietary nutritional requirement of Nile
tilapia (i.e., essential amino acids). Both short-term growth performance
and FCR were comparable to tilapia fed with fully fishmeal-based diets
(Obirikorang et al., 2015a, b). Replacement of fishmeal with palm ker-
nel in Tambaqui diets, revealed that up to 25% replacement would not
adversely affect its zootechnical performance (Silva et al., 2020). In the
case of Nile Tilapia, Yossa et al. have shown that with 30% replacement
using PKM, both protein efficiency ratio and protein productive value
showed no significant difference compared with total fishmeal-based
diet group. This proves that tilapia could efficiently digest proteins from
palm oil meal (Yossa et al., 2021).
2.2. By-products from industrial food processing
Similar to oilseed meals or cakes, by-products from industrial food
processing are discarded parts or solid residues post food production.
Common examples are soybean meal (okara), brewer’s spent grain and
yeast, etc. Considering their nutritional values and abundant annual pro-
duction, valorisation of these industrial food waste for fishmeal substi-
tution has enormous attractiveness for aquaculture.
2.2.1. Soybean meal
Soybean meal (SBM), also termed okara, is a solid residue from
soybean milk or tofu production. Production of SBM is massive. Ev-
ery year, hundred thousand tons of SBM is disposed in both Japan
(Li et al., 2013a) and Korea; while in China alone, annual production
4
Future Foods 7 (2023) 100240
of SBM could reach millions of tons (Li et al., 2012). For the world-
wide annual production, SBM amount could reach up to 1.4 billion tons
(Kamble and Rani 2020). As a by-product from soybean processing, SBM
has high nutritional values, especially protein content. It has been re-
ported that SBM dry matter contains on average 16.1% to 33.4% of
proteins (Table 1) (Li et al., 2012; Li et al., 2013a). Because of its high
protein content, SBM is one of most studied food industry by-products.
Inclusion levels of SBM in fish feed as dietary fishmeal alternative varies
from 20% for Nibea miichthioides (Huynh and Nugegoda 2011), 75%
for Nile tilapia (Huynh and Nugegoda 2011), to 100% for channel cat-
fish (Arome Ataguba, Kamble, and Salin 2017), with no interference on
their growth performances (Arome Ataguba, Kamble, and Salin 2017;
Goda et al., 2007). For African catfish, Goda et al. pointed out that 100%
substitution of fishmeal with SBM, had comparable amino acid profiles
as fishmeal-based diet of significantly higher levels of phenylalanine and
tyrosine (Goda et al., 2007). At 50% substitution of fishmeal with SBM,
orange-spotted groupers were able to maintain similar weight gain% as
that of the control without compromising survival rate (Wang et al.,
2017). Matulić et al. investigated growth performance of Ameiurus neb-
ulosus L. utilizing different inclusion level of SBM. The results revealed
that 50% inclusion had the highest weight gain% and lowest FCR values
among all groups (Matulic et al., 2020). These demonstrate the prospec-
tive of SBM as a fishmeal alternative in the future.
2.2.2. Brewer’s spent grain
Brewer’s spent grain (BSG), the main by-product obtained from beer
brewing, accounts for 85% of the total by-products produced during the
brewing process (Ikram et al., 2017; Mussatto 2014). With more than
180 million tons of global beer production, there are at least 35 million
tons of BSG generated every year (Heuzé et al., 2017). Comprising pri-
marily of grain husks, BSG is abundant in lignocellulosic components
such as lignin, hemicellulose and cellulose (Ikram et al., 2017). Nev-
ertheless, chemical analysis indicated that BSG still maintains consider-
able levels of protein, ranging from 15% to 24% by dry weight (Table 1)
(Mussatto 2014). Nazzaro et al. investigated BSG inclusion in rainbow
trout and gilthead seabream diets, and reported comparable growth
results as fishmeal-based group at 30% substitution (Nazzaro et al.,
2021). In general, rainbow trout had higher crude protein apparent di-
gestibility coefficients (ADC) than those of gilthead seabream. Jayant
et al. suggested a maximum of 50% BSG incorporation in fish feeds for
Pangasianodon hypophthalmus diet. From an economic aspect, this may
significantly reduce cost, without compromising fish growth and FCR
(Jayant et al., 2018). Such studies transpire the merit of turning brew-
ing waste (BSG) to real wealth in aquaculture, aligning with the goals
of circular economy.
2.2.3. Brewer’s spent yeast
Similar to BSG, brewer’s spent yeast (BSY) is also obtained from beer
production and accounts for the second main by-product in brewing in-
dustry (Ferreira et al., 2010). Unlike BSG, which is predominantly grain
husks, the main body of BSY is Saccharomyces cerevisiae. The nature of
BSY makes it a high-protein industrial food waste containing as high
as 40% – 50% of proteins (Table 1), with a balanced amino acid pro-
file (Marson et al., 2020). Being an organic-rich food waste, BSY has
attracted attention as a fishmeal replacement. Effectiveness of BSY with
45% substitution level in fish feed has been shown in growth trial with
Pangasianodon hypophthalmus x Pangasius bocourti (Pongpet et al., 2016).
One benefit brought by BSY inclusion in fish feeds is the improved pro-
tein level in fish after feeding. Oliva-Teles et al. determined the body
composition of seabass after partial replacement of fishmeal with BSY,
and the obtained results exhibited improved protein level in seabass
after feeding with the substituted feed. Moreover, SGR values of all ex-
perimental groups showed no statistical difference when compared to
control group, and FCR values were slightly improved with up to 30%
fishmeal substitution (Oliva-Teles and ̧alves 2001). In a study carried
out by Nguyen et al., no negative influence on growth performance and
K. Sampathkumar, H. Yu and S.C.J. Loo
survival rate of giant freshwater prawn were observed after 90 days of
feeding with different inclusion levels of BSY (maximum 60% inclusion)
(Nguyen et al., 2019). BSY is not only a cost-effective nitrogen source,
but also reported to be a nutritious feeding matter with high level of
B-complex vitamins and minerals (Ferreira et al., 2010). Supported by
these studies, the substitution of fishmeal with BSY in aquaculture diets
could be a promising waste valorisation strategy.
2.3. Challenges of direct substitution of fishmeal with food wastes
Though numerous studies have demonstrated the feasibility of uti-
lizing plant-based protein source from industrial food waste as fishmeal
alternative for aquaculture, there exist challenges and disadvantages of
plant-based protein sources. These include the presence of antinutri-
tional factors (ANFs), incomplete amino acids profiles to meet essential
growth requirement, lack of specific fatty acids, mycotoxin content and
poorer palatability (Hasan and Tan 2020). Compared to animal-based
protein source (e.g. fishmeal), the above-mentioned shortfalls of plant-
based protein source may impact fish growth adversely (Table 1).
For SFM, its fiber content and deficiency in amino acids are two ma-
jor factors that limit its further application to fully substitute fishmeal
in aquafeeds (Heuzé et al., 2019). Chemical analysis of SFM revealed
that it is deficient in Sulphur amino acids and has higher crude fiber
levels. Furthermore, high level of phenolic compounds in SFM restrict
its usage in aquafeeds (Hassaan et al., 2018). When substituted at high
levels, the existing fibers could be the reason for poor digestibility of
the feed (Hertrampf and Piedad-Pascual 2000). In feeding experiments
conducted by Olvera-Novoa et al. FCR value of tilapia fingerlings in-
creased up to 2.23 when 50% fishmeal was substituted with SFM, com-
pared to a value of 1.99 for controlled diet group. SGR value diminished
to 2.47% per day from 3.22% per day (controlled diet group) (Olvera-
Novoa et al., 2002). The author also explained that amino acids defi-
ciency in SFM may attribute to lower anabolism, leading to reduced
growth rates (Olvera-Novoa et al., 2002). For the purpose of replac-
ing fishmeal with SFM without compromising growth performance, the
recommended substitution level of SFM shall be 10% for carnivorous
fish and 20% for both herbivorous and omnivorous fish (Hertrampf and
Piedad-Pascual 2000).
Similar to SFM, the main factor that restricts complete substitution
of RM is its high fiber content and presence of ANFs (Plaipetch and
Yakupitiyage 2013; Shafaeipour et al., 2008). Though RM was found to
possess abundant minerals, especially in phosphorous, its bioavailabil-
ity was impeded due to the presence of phytic acid and fiber content
(Hertrampf and Piedad-Pascual 2000). When inclusion level of RM in
Pseudobagrus ussuriensis diet was higher than 20%, SGR value declined
drastically, from 1.3% per day to 0.7% per day. Similar trends were also
observed in terms of feeding efficiency (FE) and protein efficiency ratio
(Bu et al., 2018). Xu et al. pointed out 100% substitution of fishmeal
with RM may result in poor growth performance as well as FE for Gibel
carps. RM has been reported to be deficient in lysine and methionine,
which are two important amino acids for fish growth (Xu et al., 2019;
Luo et al., 2012). The lack of these leads to enhanced amino acids oxi-
dization and reduced FE (Xu et al., 2019). A 50%-substituted RM feed
was investigated for its effect on growth and immune response of red
sea bream, and both blood hemoglobin and serum triglyceride levels
of RM-fed fish were diminished after feeding. This indicates possibility
of physiological damage to the fish because of having RM in their di-
ets (Dossou et al., 2019). In order to avoid such outcomes, a maximum
of 10% substitution is recommended for RM in aquafeeds to achieve
comparable growth performance of fish (Hertrampf and Piedad-Pascual
2000).
SOM or sesame oil cake may have superior performance as fishmeal
substitution considering its high protein level and low fiber content.
However, lower content of lysine and high phytate levels make it un-
suitable to meet all nutritional requirement for fish growth and may
also adversely affect voluntary feed intake of fish (Nang Thu et al.,
5
Future Foods 7 (2023) 100240
2011). A SOM included diet with 25% to 75% protein replacement
level exhibited significant negative effects on common carp fry in terms
of growth rate (Nang Thu et al., 2011, Hasan et al., 1997). Mohanta
et al. investigated effects of different oilseed meal inclusion in silver
barb diet on its growth, digestibility, etc. The results demonstrated that
because of lysine deficiency of SOM, only partial inclusion of SOM (max-
imum 42%) into fish feeds could be possible, to maintain growth of fish
(Mohanta et al., 2007). Phytate can chelate metal ions to hinder reac-
tions between ingested food and its related digestive enzymes, leading
to poor feed utilization (Roy et al., 2013). By feeding rohu fingerlings
SOM containing diet with substitution levels in the range of 10% and
40%, a reduction of weight gain% and SGR were observed; from 91.82%
to 64.80%, and from 0.825 to 0.625, respectively (Roy et al., 2013). The
FCR undoubtedly increased from 1.62 for controlled diet to 2.20 for 40%
replacement of SOM in diet. This inverse correlation between SOM sub-
stitution level and growth performance was assumed to be attributed to
the presence of phytate in SOM. Existing research of SOM have eluci-
dated that presence of phytate in SOM (5%) was the major limitation
that constrained its full replacement of fishmeal. As such, inclusion lev-
els of SOM in fish feeds shall not exceed 10% for carnivorous fish and
20% for herbivorous / omnivorous fish to assure regular fish growth
performance. In addition, amino acids and minerals supplementation
should also be considered (Hertrampf and Piedad-Pascual 2000).
Compared to the aforementioned oilseed meals, PKM has a relatively
higher crude fiber level and low protein content (Hertrampf and Piedad-
Pascual 2000; Heuzé et al., 2016). Thus, PKM may not have as good a
performance as other oilseed meals in fishmeal replacement. 30% in-
corporation of PKM into Nile tilapia diet could lead to an increment of
crude fiber level to 18.99%, thereby declining their growth rate and rais-
ing FCR (Omoregie and Ogbemudia 1993). Compared to fishmeal-based
diet, 30% incorporation of PKM in Nile tilapia diet would significantly
reduce protein retention efficiency (Obirikorang et al., 2015b). With re-
spect to total ammonia-nitrogen (TAN) excretion of tilapia, 30% inclu-
sion of PKM would reduce TAN values by two folds compared to the con-
trol group (Obirikorang et al., 2015a). TAN value correlates to the types
of protein source and nitrogen intake of fish (Engin and Carter 2001).
In PKM-based diet, its lack of protein content could contribute to lower
TAN values of tilapia (Obirikorang et al., 2015a; Bonaldo et al., 2011).
Hence, a lower TAN value for PKM-fed fish could also be explained by
its deficiency in lysine and methionine (Hertrampf and Piedad-Pascual
2000).
Though SBM is available abundantly and has significant protein
value, its application in aquaculture is limited due to the existence of
antinutrients, such as protease, trypsin inhibitor, phytates, etc. (Li et al.,
2013a; Ma et al., 2019). Presence of ANFs may make feeds less palatable
to fish and can cause gastrointestinal inflammation that will adversely
affect growth (Matulic et al., 2020). Besides, methionine and cystine
deficiencies limit its total substitution for aquafeeds (Hertrampf and
Piedad-Pascual 2000; Ajani et al., 2016). In replacing fishmeal with SBM
for seabass, substitution levels of 50% could cause a decline in growth
(Ma et al., 2019). For instance, the weight gain dropped drastically from
33.94 g/fish at 30% substitution, to 8.45 g/fish at 50% substitution.
Survival rate also reduced from 100% to 60%, accordingly (Ma et al.,
2019). When feeding Australian catfish with partial SBM-replaced fish
feeds, FCR values increased for both 30% and 45% replacement. The re-
duction of apparent net protein utilization values indicated the inability
for protein digestion due to the presence of SBM (Huynh and Nugegoda
2011). Histological analysis also testified that higher inclusion of SBM
into fish feeds could lead to intestinal damage (i.e., villi fusion and twist
in intestine) because of ANFs (Wang et al., 2017).
Lastly, BSG, as a lignocellulosic by-product, has a relatively high
fiber content of up to 30% – 50% (Fernandes et al., 2022). However,
it was believed that feeding matter with fiber content less than 6% shall
be an ideal candidate for aquaculture. Studies have demonstrated that
30% substitution of BSG in fish diet could significantly impair apparent
digestibility coefficient of fish (He et al., 2020; Naylor et al., 2009). In
K. Sampathkumar, H. Yu and S.C.J. Loo
terms of nutritional value of BSG, though crude protein content can be
more than 20%, its amino acids profile is not complete and lacks cer-
tain essential amino acids needed for fish growth (lysine, methionine
and cystine) (Hertrampf and Piedad-Pascual 2000). Considering high
fiber content, the preferred inclusion level of BSG in fish feeds shall not
exceed 15% (Hertrampf and Piedad-Pascual 2000; Heuzé et al., 2017).
As for BSY, the second major by-product from brewing process, cell wall
of the yeast may impede nitrogen digestibility of fish albeit a protein-
rich food waste (Ferreira et al., 2010). Studies related to employing BSY
as protein source for aquaculture are, however, limited.
2.4. Strategies to overcome the challenges
Pre-treatment and fermentation are two different techniques being
adopted to decrease ANF and improve the protein and nutritional con-
tent of plant-based sources. Mild pre-treatment such as washing, heat-
ing and de-fatting helps to remove soluble polysaccharides and break
down complex carbohydrates and proteins thereby improving the nutri-
ent content of the meal. Apart from this, the widely used form of pre-
treatment is enzymatic hydrolysis to remove ANF and enrich the nutri-
ent content. SBM is the most commonly pre-treated plant-based protein,
owing to its abundance and high ANF content compared to other food
wastes. Based on reported studies, enzyme pre-treatment has often led
to improved growth performance and feed intake compared to untreated
samples (Liang et al., 2022). Solid state enzymatic hydrolysis could also
be a useful method to decrease the fiber content and improve the nutri-
tional value for BSG. Enzyme pretreatment for a feed based on BSG and
rice bran showed a comparable result to commercial fishmeal-based feed
for gray mullet in long term growth study (Martínez-Antequera et al.,
2022). Hydrolysis pretreatment of BSG has also been shown to improve
digestibility of gilthead seabream but did not have on effect on rain-
bow trout (Nazzaro et al., 2021). In the case of BSY, to improve its
protein utilization efficiency, the disruption of cell wall is necessary.
Common treatments utilize physical (beads agitating, ultrasonication,
high-pressure or thermolysis), chemical (alkaline or acidic solvents) or
biological (enzymatic treatments) disruptions (Marson et al., 2020). Ad-
ditional pretreatments of BSY however would increase the cost and en-
ergy consumption. Hence, seeking a more cost-effective way to enhance
BSY performance in fishmeal replacement is necessary.
Pre-treatment when combined with fermentation, has been shown
to improve nutritional profiles. Recently, Alhomodi et al. demonstrated
that a combination pre-treatment by washing and fungal fermentation
using cultures of Aureobasidium pullulans, Neurospora crassa and As-
pergillus niger greatly improved the nutritional content of canola meal
(Alhomodi et al., 2022). Co-fermentation of SBM using Bacillus sub-
tilis and Enterococcus faecium enabled about 40% replacement of fish-
meal without any significant changes to fish growth (Xu et al., 2022).
The advantages of fermentation stem from the enrichment of essential
amino acids, removal of ANF, breakdown of protein macromolecules,
which is evident from improved growth performance and feed digestibil-
ity(Nguyen et al., 2020). An additional benefit is the enhanced immune
response, mainly attributed to the presence of probiotics (Ismail et al.,
2021). Another recent study has also shown such positive effects when
Lactobacillus acidophilus was used to ferment the SBM before feeding it to
turbot juveniles (Li et al., 2022). Solid state fermentation could be a cost
effective alternative, as it minimises space requirement while serving to
enrich the microorganisms post-fermentation (Zhang et al., 2021).
Besides, pre-treatment of wastes, enzymes are also added directly to
feeds to circumvent the problem of ANF. Phytic acid or phytate is the
most common ANF for plant-based diets. Phytate is the storage form of
phosphorus in plants and phytate can form complexes with metals such
as Iron, Zinc or other minerals such as Calcium in the gastrointestinal
tract (GIT), impeding their bioavailability. Addition of phytases to fish
feed is one of the ways to reduce the ANF content. Microbial phytases
are widely used exogenous enzymes, obtained from Aspergillus niger, A.
fumigates, A. ficuum and from other fungi and yeast. Phytases help to
6
Future Foods 7 (2023) 100240
breakdown phytate, thus reducing their ANF and improve the absorp-
tion of Phosphorous, Calcium, amino acids and other metals. Vanden-
berg et al. studied the effect of inclusion of such microbial phytases
in plant-based diets using rainbow trout as a model. When the plant-
protein based diet was supplemented with 3000 FTU of microbial phy-
tase per Kg, the increase in feed efficiency, fish growth, retention of
Phosphorus and Nitrogen in tissues were comparable to those of the con-
trol diet containing fishmeal. This suggests that microbial phytase can
be used effectively to decrease the ANF of plant-based diet and increase
the digestibility and bioavailability of nutrients. The group also tried to
encapsulate phytase in a chitosan, alginate matrix, but it was observed
that encapsulation reduced the effect of the enzyme, mostly attributed
to the hampered interaction between the enzyme and dietary phytate
(Vandenberg et al., 2011). In another study, addition of phytase at 950
FTU per Kg greatly improved the growth and mineral absorption of com-
mon carp juveniles that were fed moringa seed and leaf meal based diets
(Shahzad et al., 2021). A recent review also summarises the use of ex-
ogenous enzymes in aquaculture feeds (Liang et al., 2022). This could
be an important strategy to reduce ANF and improve feed digestibility.
Similar to enzyme addition, probiotic addition to feeds has also been
shown to improve the digestibility of plant-based feeds (Gule and Gere-
mew 2022; Nathanailides et al., 2021). There are reports supporting
the positive influence of probiotics in feed on the growth and immune
response of fishes (Hai 2015; Dawood et al., 2018). The commonly sup-
plemented probiotics in fish feed are Lactobacillus sp. Bacillus sp. Entero-
coccus sp. and Pediococcus sp. A higher substitution of plant-based diet
in feed could result in damage to the intestinal mucosa leading to in-
flammation. A recent study by Nimalan et al., has shown that inclusion
of two probiotics – Lactobacillus fermentum and Lactobacillus plantarum
could alleviate inflammation and promote feed uptake (Nimalan et al.,
2022). Feed stimulants (FS) are substances that increase the ingestion of
feed by making it appealing to the fishes. Betaine, taurine, nucleotides
and nucleosides are some of the commonly used FS and are species-
specific (Lim et al., 2016). Such feed stimulants could be used in a de-
vious way for greater acceptance of plant-based feeds. Zou et al. re-
ported the successful increase in feed intake and increased feed con-
version of high plant-based diets on juvenile tilapia when substituted
with FS such as betaine, tryptophan, dimethylthetin and dimethyl-𝛽-
propiothetin (Zou et al., 2017).
While some of the strategies discussed above may help to overcome
these challenges, a complete nutritional profile can be obtained when
these strategies are combined. Some amino acid supplementations may
still be needed even after pre-treatment and fermentation. While probi-
otics improve the digestibility, poor feed palatability due to supplemen-
tation with plant-based protein may be an issue. One way could be to
mix different food wastes to optimize on their advantages. For instance,
Cao et al. prepared a blend of fermented plant meal using rapeseed meal
(RM), rice bran (RB), sprayed corn husk (SCH), palm meal (PM) and
soybean meal (SBM) in the proportion of 30:25:25:15:5. The fermented
blend significantly enhanced digestive enzyme activities, growth perfor-
mance and antioxidant capacity of juvenile Gibel carp that it was tested
on (Cao et al., 2021). Another study by Kumar et al. showed that 50%
replacement of fishmeal with enzyme pre-treated SBM together with
enzyme supplementation in diet, promoted physiological enzyme activ-
ities and growth performance against fishmeal control diet (Kumar et al.,
2019). De-fatted fermented SBM supplemented with Taurine had growth
performance similar to fishmeal-based diet in Pompano fish indicating
that a combination of these strategies could help in successful incorpo-
ration of plant-based protein in aquaculture diets (Nguyen et al., 2020).
3. Biomass conversion of food-waste consuming insects - An
Alternative protein source (Indirect substitution)
While direct substitution of fishmeal with plant-based protein is
possible, the nature of these plant-based protein sources often deters
full substitution of fishmeal. An alternative strategy is to convert these
K. Sampathkumar, H. Yu and S.C.J. Loo Future Foods 7 (2023) 100240

plant-based protein sources into more digestible forms. Apart from fer-

Devic et al., 2018; Magalhães et al., 2017;

mentation methodologies, another way is to use other organisms to di-

Rawling et al., 2012; Ngoc et al., 2016)

(Wu et al., 2020; Khosravi et al., 2018;

Hoffmann et al., 2021; Iaconisi et al.,

gest these industrial food wastes and utilize these waste-fed organisms as

Li et al., 2017; Sánchez-Muros et al.,

(Tedesco et al., 2020; Parolini et al.,

Ng et al., 2001; Jeong et al., 2022;
protein sources instead. While microalgae have demonstrated the ability

(Barragan-Fonseca et al., 2018;

to grow on waste water and assimilate the nutrients, the complexity of

2020; Musyoka et al., 2020;

different industrial food wastes, necessitates the pretreatment of wastes
(Kumar et al., 2022). In order to favor the growth of microalgae, some
treatments for industrial food wastes including thermal, chemical, or
enzymatic hydrolyses will be necessary (Kumar et al., 2022; Kim et al.,
2022). Additional pretreatments of industrial food wastes may make mi-

References
croalgae conversion strategy not sustainable and cost-effective. Besides,

2014)

2019)
microalgae-based protein source would still be regarded as a plant-based
protein. Its amino acids profile would be similar to those of soybeans
and may not meet growth requirement of fishes (Miles; and Chapman

Lower cholesterol and triglyceride levels

Amino acids deficiency in fish (taurine,

Adversely affect innate immune system

2021; Saadaoui et al., 2021). Owing to these, conversion of plant-based
industrial food wastes using microalgae may not be discussed herein.
The other strategy is to use insects to convert food waste to high nutri-

Adverse effects in aquaculture

tional value protein. This process known as insect biomass conversion

Intestinal tissue damage

alanine, leucine, lysine)

would involve feeding food waste to insects to convert them into an

Poor lipid digestibility

alternative protein source for aquafeeds. Compared to plant-based pro-
tein sources from industrial food wastes, insect meal possesses higher
protein levels. Among edible insect species that have been studied so
far, 20 of them have comparable crude protein level (60 – 80%) as
fishmeal, which is higher than plant-based protein sources (Sánchez-
Muros et al., 2014; Rumpold and Schlüter 2013). In terms of amino acid
compositions, plant-based protein sources usually lack methionine and
leucine – essential amino acids in aquaculture (Sánchez-Muros et al.,

heavy metals during

Bioaccumulation of
High level of chitin
2014). On the contrary, some species of insects, such as Bombyx mori

waste digestion
Lack of fish oil
and housefly, are reported to have higher methionine and leucine levels

Challenges
than fishmeal (Sánchez-Muros et al., 2014; Cho and Kim 2011). In ad-
dition, unlike fibrous plant-based protein sources, insect meal possesses
superior digestibility of 98.9% and 66.9% of organic matter and protein
content, respectively (Sánchez-Muros et al., 2014). Despite numerous
insects being studied for mass cultivation, the insects/worms discussed
Optimal replacement (%) Optimal FCR / FE

0.62 (FE, g/feed)

1.19 (FE, g/feed)

in the following sections were chosen based on their capability of waste 1.52 (FCR)

0.94 (FCR)

1.10 (FCR)
0.72 (FCR)

1.74 (FCR)
1.08 (FCR)
treatment and potential as protein sources in fish feeds. For instance,
2.1 (FCR)

Black soldier fly has been intensively studied for years because of their
rapid digestion of organic food wastes and high protein level. Mealworm

-
-
has the advantage that it can digest both food and plastic wastes. Fur-
Protein content of insects / worms for fishmeal substitution and possible adverse effects.

100% (combination with

Provide 66.35% protein

thermore, earthworms have been conventionally used for composting of
100% (defatted BSFL)
19.5% (45% fishmeal

food wastes.
vermicompost)
replacement)

3.1. Types of insects for fishmeal substitution

80 g/kg

in feed

3.1.1. Black soldier fly

16%
40%
60%
10%
70%
30%

In global insect farming, Hermetia illucens, also called black soldier

fly (BSF), is one of the most common insects for potential application
Acanthopagrus schlegelii

as animal feeds. This has been attributed to the ability of BSF to feed
on a variety of feeding substrates including kitchen wastes, chicken ma-
Sebastes schlegeli

Cyprinus carpio

nure and even human feces (Lalander et al., 2019; Nguyen et al., 2015;
Fish species

Nile tilapia

Nile tilapia

Zhou et al., 2013; Banks et al., 2014). As BSF will not eat during the
Jian carp

Sea trout
Seabass

Catfish

adult fly stage, the larvae stage of BSF is therefore of importance here

Trout
Carp

(Lalander et al., 2019). Nutrition wise, black soldier fly larvae (BSFL) has
a crude protein level of around 50% (Table 2) (Barragan-Fonseca et al.,
2018), and is abundant in minerals such as phosphorous and calcium
Protein content

73% (defatted)

(Fitriana et al., 2021). Fitriana et al. analyzed the influence of different

feeding substrates (organic wastes) on nutrient composition of BSFL and
54.6%

revealed that protein content of BSFL was relatively stable when fed with
50%

52%
(%)

different feeding substrates (i.e., SBM, brewer’s grain, etc.). Though the
nutrient composition of BSFL was not affected by feeding larvae with
Mealworm (Tenebrio

Earthworm (Eisenia
(Hermetia illucens)

different wastes, growth rate and biomass increment of larvae varied

Insects / Worms

Black soldier fly

molitor) larvae

with different feeding substrates (Fitriana et al., 2021). Similar results

were also observed in a study carried out by Mirwandhono et al., where
Table 2

different fermented agricultural waste – such as rice bran or PKM – had

fetida)
larvae

no significant effects on nutrient composition of BSFL in terms of pro-

tein, fat and carbohydrates (Mirwandhono et al., 2022). In view of this,

7
K. Sampathkumar, H. Yu and S.C.J. Loo
BSFL could potentially be used to convert industrial food waste into a
high protein feed additive for aquaculture.
Devic et al. investigated the inclusion of BSFL in fish feeds on growth
performance and feed utilization on Nile tilapia (Devic et al., 2018).
Within the BSFL inclusion range tested, BSFL-enriched fish feeds ren-
dered statistically higher survival rates after 32 days of feeding trial.
FCR, protein efficiency ratio and crude protein content were comparable
among all inclusion levels tested (Devic et al., 2018). The most promi-
nent change was fatty acid levels with differing BSFL inclusion levels.
Compared to fishmeal-based diet, BSFL meal is rich in n-6 fatty acids
but less in n-3 fatty acids. With more inclusion of BSFL into diet dur-
ing feeding of tilapia, n-6 polyunsaturated fatty acids increased in fish
fillets, whereas n-3 polyunsaturated fatty acids decreased (Devic et al.,
2018). In feeding trial with seabass, a maximum of 19.5% inclusion
of BSF pre-pupae would not negatively affect feed efficiency and daily
growth rate. High apparent digestibility coefficients indicated BSF pre-
pupae could be well digested by seabass (Magalhães et al., 2017). When
defatted BSFL was substituted into fish feeds, no obvious difference of
growth performance or FCR of juvenile carp was exhibited with maxi-
mum 100% replacement of fishmeal (Li et al., 2017), implying the strong
potential of BSFL as a fishmeal alternative in aquaculture.
3.1.2. Mealworm
In addition to BSFL, mealworm larvae (Tenebrio molitor) is another
promising candidate for both waste treatment and fishmeal replace-
ment. Similar to BSFL, mealworm larvae also possess around 52% crude
protein level (Table 2) which could be an ideal protein source for
aquafeeds (Wu et al., 2020). Most importantly, the protein from meal-
worm larvae contains amino acids such as taurine (0.34 mg), methionine
(6.01 mg) and cysteine (11.86 mg) (per gram of dried larvae), which is
lacking in plant-based protein sources (Wu et al., 2020). In addition to
high-quality protein of mealworm larvae for aquafeeds, the presence of
oleic acid and phospholipids in mealworm larvae are a good source of
lipids (Wu et al., 2020). One extraordinary advantage of mealworm is
its broad range of diets, from organic wastes to petrochemical plastic
wastes such as polystyrene (Yang et al., 2018; Yang et al., 2015) and
polyethylene (Przemieniecki et al., 2022).
In terms of organic waste digestion, mealworm undoubtedly ex-
hibits great digestibility towards most industrial food wastes. Yang
et al. investigated the ability of mealworms to digest different types
of lignocellulosic wastes, and mealworm larvae could be fed on rice
straw, rice bran and corn straw without compromising its survival rate
(Yang et al., 2019). When changing mealworm diet from conventional
wheat bran to SBM, crude protein level of mealworm larvae increased
from 68.93% to 74.43%, without affecting their amino acids profile
(Zhang et al., 2019). Similar observation was also reported when its diet
was switched to RM, with unaffected survival rate and comparable FCR
values (Bordiean et al., 2020). As a high protein content food waste,
BSG was also well digested by mealworm larvae with no negative ef-
fects on both survival rate and development time (Oonincx et al., 2015).
Apart from impressive digestibility to various food wastes, mealworm
larvae were also favored for aquaculture application due to its nutri-
tional value. Compared to control group (fishmeal-based diet), increas-
ing inclusion amount (maximum 16% inclusion) of mealworm meal to
the diet of Sebastes schlegeli with methionine supplementation could im-
prove growth performance of fish such as SGR and weight gain. Meal-
worm inclusion without addition of methionine still showed comparable
growth performance as fishmeal-based group (Khosravi et al., 2018). By
adding 40% of mealworm larvae into catfish diet, Ng et al. demonstrated
that no adverse effects on growth performance or feed utilization rate
was observed, even up to 80% (Ng et al., 2001). Jeong et al. found that
with up to 60% fishmeal substitution with mealworm, growth perfor-
mance of Acanthopagrus schlegelii exhibited similar result as the control
group (Jeong et al., 2022). In a study of fishmeal replacement with meal-
worm meal for sea trout, 10% replacement rendered the best growth per-
formance for fish in terms of FCR, SGR, etc. while at 40% replacement,
8
Future Foods 7 (2023) 100240
survival rate of fingerlings still could be maintained at 95%. Signifi-
cantly, histomorphological analysis of fish intestine and liver confirmed
the safety of mealworm meal inclusion in sea trout diet (Hoffmann et al.,
2021).
3.1.3. Earthworm
The role of earthworm (Eisenia fetida) in composting and ameliorat-
ing soil quality is notable. Though earthworm is not classified as “insect”
in taxonomy aspect, its importance in both industrial food waste decom-
position and animal feed application are highly estimated. Earthworms
tend to have a voracious appetite towards different types of food wastes.
The process of earthworm digesting organic matters (food wastes) and
decompose them into high-quality compost is called vermicomposting.
By vermicomposting, these wastes could be biodegraded with less emis-
sion of Greenhouse Gas (GHG) and nitrogen loss compared to conven-
tional composting process (Tedesco et al., 2019). Sharma et al. demon-
strated that the levels of organic matter in waste, declined after vermi-
composting, while levels of nitrogen, potassium as well as phosphate
were significantly enhanced (Sharma and Garg 2017). Zhang et al. in-
vestigated using earthworm for decomposition of okara and resultant
vermicompost showed excellent effects on vegetable (Choy Sum) growth
(Zhang et al., 2021). In study of vermicomposting of rice straw, nitrogen,
phosphate and potassium levels in compost were improved, and organic
carbon as well as carbon-nitrogen ratio were contrarily reduced with
no compromise on earthworm growth and reproduction (Sharma and
Garg 2018). Hanc et al. employed earthworm for decomposing a mix-
ture of spent coffee grounds and straw pellets. The results illustrated po-
tency of earthworm in reducing caffeine content in spent coffee grounds
(Hanc et al., 2021), providing a promising way to bioconvert spent cof-
fee grounds into an animal-based protein. In the application as animal
feeds, earthworm is regarded as nutritious for animal feeds consider-
ing its high quality and quantity of protein content, with at least 54.6%
protein dry matter (Table 2) (Tedesco et al., 2020). Tedesco et al. de-
termined nutritional values of earthworm after feeding with fruit and
vegetable wastes, the protein level of defatted earthworm could reach
as high as 73% (Table 2), and so did minerals content (potassium and
calcium) (Tedesco et al., 2020). As for amino acids profile, earthworm
is reported to have high content of essential amino acids like lysine
and methionine, which are similar or even slightly higher than fish-
meal (Parolini et al., 2020). Earthworm meal was reported to be able
to improve protein digestibility of carp and with up to 30% inclusion
in trout diet, with no adverse effects on growth rate and FCR reported
(Parolini et al., 2020). The replacement of fishmeal with mixture of
earthworm meal and vermicompost for tilapia revealed no negative in-
fluence on survival rate or FCR of fish with up to 100% replacement,
indicating the possibility of earthworm meal as a sustainable fishmeal
substitute (Musyoka et al., 2020). When Cyprinus carpio were fed with an
earthworm (Perionyx escavatus) meal included diet (66% protein from
earthworm), weight gain of fish after a 60-day feeding trial was elevated
compared to fishmeal-based or SBM-supplemented diet (Rawling et al.,
2012), proving the superiority of utilizing earthworm meal in aquacul-
ture.
3.2. Challenges of inclusion of insect meal in fish feed
Insect meal has manifested its superiority for fishmeal substitution
compared to direct substitution with plant-based industrial food waste,
as evident from the former’s nutritional profile. The bioconversion of
industrial food wastes into a protein source by insect digestion provides
an indirect way for waste valorisation, thus achieving a circular econ-
omy. Nevertheless, there are still some limitations that could limit the
use of insect meal in aquaculture (Table 2). For instance, the relatively
high level of chitin in insects, lack of fish oil and potential enrichment
of heavy metals in insects after waste digestion. Chitin is an indigestible
polysaccharide, which is abundant in exoskeleton of insects. Presence of
chitin in feed may influence protein digestibility (Sánchez-Muros et al.,
K. Sampathkumar, H. Yu and S.C.J. Loo
2014). Low chitin level in fish feeds may promote fish growth by ele-
vating Bifidobacterium in fish gastrointestinal tract whereas higher lev-
els of chitin in feed may impede protein and lipid digestion (Sánchez-
Muros et al., 2014). Insect meal may not have comparable fatty acid
profiles as fish oil, which may affect fish fillet quality due to reduced
n-3 fatty acids in fish muscles (Sánchez-Muros et al., 2014). It is also
possible that heavy metals in organic wastes may be bioaccumulated
in insects/earthworms which may be passed to the fish (Parolini et al.,
2020), resulting in food safety issues.
Some adverse effects of insects or earthworms in fish feeds have been
previously reported. For instance, Li et al. discovered that a higher than
75% fishmeal replacement with defatted BSFL meal, intestinal tissue
damage was observed in juvenile Jian carps due to chitin and its deriva-
tives (Li et al., 2017). Higher BSFL meal inclusion also resulted in de-
creasing n-3 polyunsaturated fatty acids (PUFA) and increasing levels
of n-6 PUFA, thus affecting the quality of the fish fillet (Devic et al.,
2018). In studies using mealworm larvae, even at low levels of sub-
stitution (25%), taurine deficiency for gilthead sea bream was reported,
whereas a significant reduction in essential amino acids such as alanine,
leucine and lysine was observed for rainbow trout (Iaconisi et al., 2019).
A diet with higher than 11% fishmeal replacement using mealworm lar-
vae caused a downward trend for total cholesterol and triglyceride levels
in largemouth bass. Again, chitin inhibited the nutritional performance
of the feeds (Jeong et al., 2022). Similar negative effects were also ob-
served when earthworm meal was introduced into fish diets.
Rawling et al. reported that inclusion of earthworm (Perionyx es-
cavatus) meal may adversely affect response of innate immune system
of Cyprinus carpio despite superior performance of earthworm meal in
achieving higher weight gain after feeding (Rawling et al., 2012). 100%
replacement of fishmeal with earthworm meal for carp diet showed re-
duced lipid digestibility, declining from 87.8% for fishmeal-based diet
to 75.2% for earthworm meal-based diet. A similar trend was also ob-
served for growth performance of carp when replacing all fishmeal with
earthworm meal (Ngoc et al., 2016). In terms of fatty acid profiles, earth-
worms are lower in docosahexaenoic acid (DHA), an essential long chain
PUFA for fish growth, regardless of its abundance of other long chain
PUFA such as eicosapentaenoic acid (EPA) (Kumlu et al., 2018). Neces-
sary enrichment of DHA in earthworm-based meal should be considered
in order to achieve a good growth performance in fishes.
In addition to nutritional and food safety aspects, using waste-fed
insects/earthworms may potentially increase the cost compared to di-
rect substitution with industrial food wastes for fishmeal replacement,
or using fishmeal in aquafeeds directly. Though limited data is avail-
able for assessing cost of using earthworms for fishmeal replacement,
some preliminary studies have revealed obviously higher cost of using
earthworms for aquaculture applications compared to those of conven-
tional protein sources (Parolini et al., 2020). Thevenot et al. evaluated
costs for production of 1 kg of mealworm larvae meal in terms of energy
consumption, GHG emission, land use, etc. For production of each kg of
protein from mealworm larvae meal, the costs were higher than those of
equal amount of protein out of SBM or fishmeal (Thévenot et al., 2018).
Not only is the economic impact of replacing fishmeal with insect meal
high, but also public acceptance towards insects application in aquacul-
ture feeds would be an issue (Le Féon et al. 2019). Customers may not be
inclined to accept insect meal-fed fish, especially using waste-fed insects
(Le Féon et al. 2019). At scientific level, waste-fed insects as fishmeal
substitution could valorise industrial food waste effectively and boost
sustainable aquaculture production. However, it still has a long way to
go from scientific research to being put in practice.
3.3. Strategies to overcome challenges
The major challenge in the use of insects in feed as outlined as above,
is the presence of chitin. Higher amounts of chitin in the insect ex-
oskeleton can reduce the ADC of feed and can potentially be harmful to
fish at high substitution rates. Reducing chitin content through physical
9
Future Foods 7 (2023) 100240
removal of exoskeleton is one way to eliminate chitin. But the process
is costly. Another method is by biological reduction using chitinolytic
enzymes. This could be done by direct bacterial fermentation or enzyme
treatment of the insect meal. Nafisah et al. have shown the successful
use of Bacillus subtilis to breakdown the chitin in BSFL by fermentation
and reduce the crude fiber content from 20% to 13%, making it more
digestible (Nafisah et al., 2019). A study by Banerjee at al identified
at least 34 potent strains that possess chitinolytic properties in the GIT
of carps. The isolation and supplementation of such probiotic stains in
feed could be an alternative to improving the feed digestibility when
supplementing with insect meal (Banerjee et al., 2015). In addition to
improving the digestibility of feed, probiotics can also help to complete
the fatty acid profiles. Supplementing the feed with probiotics like Vib-
rio spp. which have been isolated from fish gut and shown to produce
PUFA like EPA and DHA would make up for these essential fatty acids,
that are absent in insect meals (Ringø et al., 1992; Ringø et al., 1992;
Yano et al., 1994). An alternative to improve the nutritional profile of
insect meal could be to supplement the diets of the insects in addition
to the industrial food waste. For instance, BSFL diet was supplemented
with colza oil or fish offal in addition to SBM to optimize the PUFA levels
suitable for growing Nile Tilapia. The results showed that BSF prepupae
fed with colza oil could not only successfully accumulate the required
PUFA, but is also cost effective (Gougbedji et al., 2021).
Use of micro algae in fish diet has been shown to remove the toxic
effects of heavy-metal contaminants when present in sub-lethal doses. A
recent review by Latif et al. summarises the different studies that used
Spirulina and other microalgal species to alleviate the effects of con-
taminants in freshwater fish (Abdel-Latif et al., 2022). Sherif et al. have
shown that supplementing the feed of Tilapia with 5 to 10 g Spirulina
algae Arthrospira platensis per Kg of feed could help to decrease mortal-
ity rate and improve the immunity due to lead nitrate contamination
(Sherif et al., 2020). In another study that investigated the protective
role of Spirulina platensis on Cadmium treated Clarias batrachus, it was
found that supplementing the feed with 10% Spirulina could improve
the immune parameters. This was mainly attributed to the phycocyanin
in spirulina, which is a potent antioxidant. It was also postulated that
the Carotenoid pigment of Spirulina could maintain the integrity of mu-
cous membrane of the GIT thereby preventing the entry of toxic ele-
ments into the body (Pundir 2019). While the studies show the ability
of microalgae as a potential solution to combating heavy metal con-
tamination in fishes, it may not prevent the transmission of these con-
taminants into humans through the food chain. Hence, more research
should be directed at preventing this bioaccumulation of heavy metals
or to sequester them from the insects before adding them to feeds.
4. Functionalised feeds using encapsulation techniques
In order to complete the nutritional profile and improve the feed
performance of feeds produced from waste, feed functionalisation could
be a possible way to matchup to fishmeal-based feeds. All encapsula-
tion systems that have been reported so far, might be applied to fish
feeds depending on the end application (Masoomi Dezfooli et al. 2019).
This section focuses on studies that have specifically used or with the
intention of using such delivery systems in aquaculture feeds. As dis-
cussed in Section 2.4, probiotics are an excellent way to improve feed
digestibility, enhance growth and immunity in fishes, while maintain-
ing water quality. But due to their labile nature, they also face the
challenge of being lost during the feed manufacture, handing and stor-
age process or even within the GIT tract of fishes before reaching the
intended site of action. Encapsulation could be one of the better op-
tions to protect the viability of the probiotics in different adverse en-
vironments. For instance, Lactobacillus plantarum isolated from the gut
of freshwater catfish was encapsulated in alginate matrices and was
found to be effective against S. agalactiae and other common food borne
pathogens in vitro. The encapsulation matrix was able to protect the pro-
biotic at a temperature of 50 °C for 1 h, showcasing the importance of
K. Sampathkumar, H. Yu and S.C.J. Loo
encapsulation. Such heat stable encapsulation could ensure that the pro-
biotics could be successfully incorporated into feed pellets using a pel-
letiser (Kumaree et al., 2015). Similarly, another study using alginate
and prebiotics from Jerusalem artichoke for encapsulation showed im-
proved survivability of the probiotic bacteria Lactobacillus rhamnosus GG
(LGG) during pelletising and also when exposed to simulated gastric and
intestinal fluids (Sribounoy et al., 2021)
Ascorbic acid (AA) is a micronutrient known to improve immunity
but cannot be synthesised by fishes. When added to feeds directly, it
faces potential degradation due to light, heat and environmental factors.
Luis et al. have shown that nanoencapsulation of AA using chitosan and
polycaprolactone could help to prevent the degradation of the nutrient.
In vivo studies in zebrafish have shown that polycaprolactone nanopar-
ticles of size 300 nm loaded with AA had an LC50 value of 179.6 mg/ml
indicating their tolerability (Luis et al., 2021). Microencapsulation is be-
ing used as a tool to not only deliver nutrients to fishes, but also to tackle
nutrient deficiencies in humans, by translating the nutrients from fish
to humans directly. Based on a recent study by Willer et al. Vitamin A
and D fortified BioBullets (patented lipid-walled microcapsule formula-
tion) could be successfully ingested by oysters and accumulated in their
tissues. At 3% loading, the bioaccumulation of Vitamin A and D were
997 and 47 𝜇g 100 g−1 , respectively, which is much higher than that in
Salmon. It is hypothesised that this could then be translated to humans
when consumed (Willer and Aldridge 2020). Amino acid supplementa-
tion to make up for essential amino acids that are not part of the plant-
based diet, has become common practice. But the added amino acids,
tend to leach out in the tanks leading to loss of the nutrient and mak-
ing the feed incomplete. As an attempt to solve this problem, Manish et
al. encapsulated methionine in lipid-based particles to supplement this
essential amino acid in feeds and prevent leaching. In vivo pharmacoki-
netic studies in Tilapia showed that encapsulation could indeed prevent
leaching and burst release, sustaining the level of methionine in plasma
for longer duration (Mahotra et al., 2022).
Taste and flavor masking of insect meal is an important step towards
its seamless integration into animal protein. In this regard, Sanchez et al.
used a well-known encapsulation matrix to mask house fly larvae meal
(FLM). FLM has a high protein (54%) and lipid (22%) content, high in
essential amino acids and unsaturated fatty acids. It could be a valuable
substitute for fishmeal. In order to improve the organoleptic properties
of FLM, it was spray died using Alginate and maltodextrin resulting in
mono-dispersed micron-sized powder. The powders better masked the
odor of the meal compared to non-encapsulated FLM (Sánchez et al.,
2021).
5. Regulation, public perception, and acceptance of waste fed fish
Regulations for feed preparation of fish is much more relaxed com-
pared to the other animal proteins. As for using industrial food wastes,
there are no stringent regulations, except that the prepared feed should
meet the existing safety standards (Mo et al., 2018). Insects from the
wild have been traditionally included as part of the diet for centuries
in some cultures around the world, especially in Asia, South America
and Africa. With the recent interest in farming insects as an alternative
protein source, there has been an increase of such producers focusing on
BSFL, mealworms and crickets. While the legislation for insect in food
is still quite vague and evolving, some countries are making provisions
to include them. Insects are categorised as novel foods in Europe and
Canada following a recent legislation. The feed used to rear the insects
is the main constraint as it might transmit some diseases into the food
chain like spongiform encephalopathies (Hawkey et al., 2021).
There are strict regulations for using insects as feed for farmed an-
imals in the European Union (EU). The rearing and use of insects such
as Black soldier fly (H. illucens), Yellow Mealworm (Tenebrio molitor),
Lesser Mealworm (Alphitobius diaperinus), Common Housefly (Musca do-
mestica), House cricket (Acheta domesticus), Banded cricket (Gryllodes
sigillatus) and Field Cricket (Gryllus assimilis) as a feed for aquaculture
10
Future Foods 7 (2023) 100240
animals has been approved in the EU. Mainly, Insects intended to be
used as food/feed must be fed materials of plant origin only. It is the re-
sponsibility of feed producers to ensure the origin of insects before use.
In addition, protein derived from insect source is approved to be used
as an additive in aquaculture. But, the processed insect protein requires
a health certificate based on the feed substrate and rearing conditions
(Mohan et al., 2022).
In the United States, edible insects are listed as food additives unless
they are generally recognised as safe (GRAS) substances by Food and
Drug Administration (FDA) (Lähteenmäki-Uutela et al., 2018). Specifi-
cally, only BSFL can be included in animal feed, limited to use in aqua-
culture feeds for Salmonid family of fishes. Canada is still cautious by
listing insects as novel foods, which are those ingredients that do not
have a history of safe use. In 2017, after rigorous consideration based
on the different insect species, substrate used as feed and the rearing
condition, BSFL was approved for use in aquaculture (Lähteenmäki-
Uutela et al., 2021). Based on some surveys done in specific countries,
acceptance of the use of insects is positive at least in aquaculture. Since
safety would be the determining factor when adopting new practices,
insect farmers should also ensure utmost care to biosecurity.
In addition to policy making and clear legislation, public perception
and acceptance is a major determinant to bring forward such unconven-
tional feed additives to common practice. Having said that, information
dissemination is crucial to get the right information across to the public
to remove any erroneous misconceptions and help them make an in-
formed decision. With all the above done right, the sensory aspect of
fish produced through these sustainable methods is the deciding factor
in its public acceptance. While incorporation of industry food wastes
directly into the feed, may not greatly affect the taste or smell in a neg-
ative way, this may not be the case for indirect substitution using insects.
Some sensory tests have been conducted previously to compare the ef-
fects of insect meal (BSF prepupae and TM larvae) substituted feed, on
the flavor, texture and aroma of meat (Sogari et al., 2019). A study by
Borgogno et al. found a distinct metallic flavor in the fish that were fed
BSFL based diets, but no off- flavor was observed (Sealey et al., 2011).
Belghit et al. reported changes in the texture and flavor of the rainbow
trout fillets depending on the inclusion level of BSFL in the diet. With
higher inclusion levels (25%, 50%) there was a dominance of metallic
flavor but decrease in fibrous nature of the fillet (Borgogno et al., 2017).
The taste perception may vary hugely between populations and detailed
studies are required before marketing such food products (Piha et al.,
2018).
6. Conclusion and future perspectives
While it has been accepted that formulated feed and farmed fish is
one pivotal way to meet the global demand for food fish, it is impor-
tant to do it sustainably. Valorisation of food industry by-products is
a promising option as presented in the discourse above. Though 100%
replacement of fishmeal may not be possible immediately, research in
this area has shown promising results.
• Promising results have been presented for less than 50% direct re-
placement of fish meal with industry food waste such as SFM, SOM,
PKM, SBM and BSG. The biggest problem is the digestibility and
palatability especially when fed to carnivorous fish.
• Higher substitution rates could be possible when combining different
industrial food wastes.
• Similarly, less than 50% indirect replacement of fishmeal with waste
fed insect meal, have shown good results with improved digestibility
and low FCR, observed for most studies.
Future studies aiming to close the gaps in reaching 100% replace-
ment should be aimed to complete the nutritional profile, improve the
feeding intake while reducing the anti-nutritional factors. Successful
translation of the research carried out in the field also requires rigor-
ous studies on any risks involved in consumption of waste-fed fishes,
K. Sampathkumar, H. Yu and S.C.J. Loo
changes to national policies and information dissemination on the safety
and advantages of food produced by such methods. Cost is another im-
portant consideration in terms of feed preparation. Cost of the feed may
not be significantly altered, as any cost reduction, via the replacement
of fishmeal, will be offset by waste processing. Supplementing feeds to
achieve a complete nutritional profile may also further increase cost.
Hence, policy making to support sustainable practices, with additional
incentives, would provide the impetus for farmers to embrace alterna-
tive protein feeds. It is undeniable that the cost involved when tran-
sitioning from conventional practices to new sustainable approaches
could be high at the beginning. But if the benefits far outweigh the costs,
then this will be one attractive method for stepping into our sustainable
future.
Statements & declarations
Funding
The authors would like to acknowledge the financial support from
the Singapore centre for Environmental Life Sciences Engineering
(SCELSE) (MOE/RCE: M4330019.C70), Ministry of Education AcRF-
Tier 1 grant (RG19/18 and RT08/19), the Singapore National Biofilm
Consortium (SNBC/2021/SF2/P04) and the Singapore Food Agency
(SFS_RND_SUFP_001_06).
Ethical statement
The research presented does not involve any human or animal study.
Statement of novelty
The surging global population has increased the demand for food
supply which is expected to nearly double in the next thirty years. Food
fish, an important source of protein, has made aquaculture one of the
key players in meeting the demands of the global food supply. This has
also led to the increase in demand for fish feed raw materials such as
fish meal and fish oil. Fish meal is a finite resource and identifying sus-
tainable alternatives to it, would be one of the key ways to keep the
aquaculture industry growing. Numerous industrial food wates are rich
in protein and could be excellent alternatives to fish meal in terms of
protein content. Currently, a focused review on the different strategies
in utilizing industrial food wastes for aquaculture is lacking. In view of
this, the review provides an overview on the use of different industrial
food wastes, both directly and indirectly in aquaculture feeds. A dedi-
cated section on using encapsulation techniques to improve the quality
of fish meal substituted feeds is also presented. Such insights would help
the readers to understand the current status of fishmeal replacements
and bridge any gaps in the field.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
CRediT authorship contribution statement
Kaarunya Sampathkumar: Conceptualization, Writing – origi-
nal draft. Hong Yu: Conceptualization, Writing – original draft.
Say Chye Joachim Loo: Funding acquisition, Writing – review & edit-
ing.
Data availability
No data was used for the research described in the article.
11
Future Foods 7 (2023) 100240
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