Waste Management 115 (2020) 95–112

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Waste Management
journal homepage: www.elsevier.com/locate/wasman

Fish and fish waste-based fertilizers in organic farming – With status

in Norway: A review
Ishita Ahuja a,⇑, Egidijus Dauksas b, Jannicke F. Remme c, Roger Richardsen d, Anne-Kristin Løes a
a
Norwegian Centre for Organic Agriculture (NORSØK), NO-6630 Tingvoll, Norway
b
Department of Biological Sciences, Norwegian University of Science and Technology (NTNU), Ålesund, Norway
c
SINTEF Ocean, Ålesund, Norway
d
SINTEF Ocean, Tromsø, Norway

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

Article history: This paper reviews relevant knowledge about the production and uses of fertilizers from fish and fish
Received 22 May 2020 waste (FW) that may be applicable for certified organic farming, with a focus on crop and horticultural
Revised 8 July 2020 plants. Fish industries generate a substantial amount of FW. Depending on the level of processing or type
Accepted 14 July 2020
of fish, 30–70% of the original fish is FW. Circular economy and organic farming concepts were used to
evaluate the potential of production of fertilizers from captured fish. Fertilizers produced from captured
fish promote the recycling of nutrients from the sea and back to terrestrial environments. Nutritional
Keywords:
composition of FW is assessed to determine the potential to supply plant nutrients such as nitrogen,
Anaerobic digestion
Circular economy
or a combination of nitrogen and phosphorous, or to enrich a compost. Methods used in processing of
Fertilizer FW to produce fish- emulsion, fish hydrolysate/fish silage, fish-compost and digestate from anaerobic
Fish industries digestion/co-digestion are presented. Using information about commercially available fish-based fertiliz-
Fish processing ers listed by the Organic Materials Review Institute (OMRI), we present a scenario for establishing fish/
Nutrients recycling FW-based fertilizers industry and research in Europe. With Norway’s 9th position among top ten global
capture producers and focus in Norway on developing organic farming, we brief how FW is currently uti-
lized and regulated, and discuss its availability for possible production of FW-based organic fertilizers.
The amount of FW available in Norway for production of fertilizers may facilitate the establishment of
an industrial product that can replace the currently common use of dried poultry manure from conven-
tional farming in organic farming.
Ó 2020 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
2. Organic* farming, nutrients recycling and circular economy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3. Nutrients in fish and FWs suitable as crop fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
4. Processing of fish/FW for use as feed or fertilizer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
4.1. Fish emulsion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
4.2. Fish hydrolysate (fish silage) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
4.2.1. Fish hydrolysate(s) through enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
4.2.2. Acid fish silage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
4.3. Fish compost . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
4.4. Anaerobic digestion of FW and possible use of biogas digestate as fertilizer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
5. The OMRI, OMRI-allowed fish-based fertilizers products, and applicability. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
5.1. About OMRI, and the OMRI’s Canada program . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
5.2. Commercially available fish-based fertilizers listed by OMRI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
6. Scientific studies related to commercially available fish-based fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
7. Effect of FW-based non-commercial fertilizers on plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106

⇑ Corresponding author.
E-mail address: ishita.ahuja@norsok.no (I. Ahuja).

https://doi.org/10.1016/j.wasman.2020.07.025
0956-053X/Ó 2020 Elsevier Ltd. All rights reserved.
96 I. Ahuja et al. / Waste Management 115 (2020) 95–112

7.1. Effect of FW-based liquid fertilizers on plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106

7.2. Effect of FW-based compost on plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
8. The fishing industry and FW-utilization in Norway. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
8.1. Norwegian fishing industry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
8.2. Utilization of FW to produce marine ingredients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
8.3. Potential for utilization of FW as fertilizers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
9. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
Declaration of Competing Interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
Appendix A. Supplementary material . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109

1. Introduction 2017). FW, as a by-product of fish markets/fish processing indus-

The fishery industry is economically important in many coun-
tries including China, India, Spain, the US, Canada, and Norway
(Aster, 2018; FAO, 2020; Kazemi et al., 2017). From 2007 to
2017, the world’s total production of fish (fisheries and aquacul-
ture) increased with a compound annual growth rate of 2–3.5%
(Aster, 2018). The world’s total fisheries and aquaculture produc-
tion in 2018 was 178.5 million tonnes, of which capture fisheries
accounted for around 96.4 million tonnes (FAO, 2020). The increase
in global capture fisheries (5.4% from the average of past three
years) was mainly driven by marine capture fisheries, due to an
increase in production from 2017 to 2018. In 2017, the production
was 81.2 million tonnes, and in 2018, it was 84.4 million tonnes.
The global capture fisheries (long-term) have been rather stable
since late-1980 s, with catches usually fluctuating between (86
million tonnes
93 million tonnes per year), with exception in
2018 (96.4 million tonnes) (FAO, 2020).
After China, Norway is the second major exporter of fish and
fish products (in 2018: China (14%) and Norway (7%). Catches by
Norwegian fleet include big volumes of cod, herring, mackerel
and other whitefish and small pelagic species (FAO, 2020;
Richardsen et al., 2019).
Raising, catching, and processing of fish leads to vast amounts
of wastes, which are of global concern (Caruso, 2016; Choe et al.,
2020; Feltes et al., 2010; Harikrishna et al., 2017; Villamil et al.,
2017). For each tonne of fish consumed, about the same amount
of fish waste (FW) is discarded by ocean dumping or land disposal
(Dao and Kim, 2011; Illera-Vives et al., 2015a; Karim et al., 2015;
Pfeiffer, 2003).
The term ‘‘fish waste” may include different materials such as
whole fish (dead or damaged fish), fish trimmings, and specific tis-
sues, such as heads, intestines, tails and fins, skins, scales, and
bones etc. Different studies have used different terms, for example,
‘‘fish waste”, ‘‘fish processing waste”, ‘‘by-products”, ‘‘raw materi-
als” or ‘‘rest raw materials” (Choe et al., 2020; Dominy et al.,
2014; Estevez et al., 2014; Ghaly et al., 2013; Kannan et al.,
2017; Lopes et al., 2015; Olsen et al., 2014; Richardsen et al.,
2019; Rustad et al., 2011; Sahu et al., 2014; Sahu et al., 2016;
Shaviklo, 2015; Toppe et al., 2018). From the studies describing
production of fertilizers from FW, we found ‘‘fish waste” to be
the most commonly used term (Abbasi, 2011; Balraj et al., 2014;
Carney et al., 2000; Dao and Kim, 2011; Illera-Vives et al., 2017;
Radziemska et al., 2018; Toppe et al., 2018; USDA, 2019a). There-
fore, in this review, mostly, we have used the term ‘‘fish waste”,
but at some places, by-products/raw materials/rest raw materials
(as such have been also used).
Large amounts of FW are produced in the main capture fisheries
countries, such as Canada, USA, India, Republic of Korea, China,
Spain and Norway (Balraj et al., 2014; Estevez et al., 2014; FAO,
2020; Ghaly et al., 2013; Kazemi et al., 2017; López-Mosquera
et al., 2011; Sahu et al., 2016; Teh and Sumaila, 2013; Xu et al.,
tries, depending on the conversion, may represent 30–45% of the
original weight of the product (Illera-Vives et al., 2015b; Kazemi
et al., 2017; Teh and Sumaila, 2013). FW depending on fish pro-
cessing and non-utilization, most likely can represent about 30 –
70% of the original fish (Toppe et al., 2018). The amounts of FW that
can be generated due to fish processing, as mentioned in different
studies, are described in Table S1.
Utilization and further processing of FW are dependent on the
local conditions and the structure of the industry. For food, feed,
technical and pharmaceutical purposes, FW may be processed to
proteins, amino acids, peptides, collagen, oil, minerals, enzymes,
flavours, and other compounds (Eilertsen et al., 2017; Ghaly
et al., 2013; Rustad et al., 2011). FW that does not meet relevant
standards for food or feed, may be used for energy production or
fertilizers (Dao and Kim, 2011; Fernandez-Salvador et al., 2015a,
2015b; Toppe et al., 2018; USDA, 2019a; Ward and Løes, 2011).
The use of FW for production of fertilizers has received atten-
tion over the years to increase the economic and ecological sus-
tainability of the fish industry (Aung and Flick, 1980; Beckley
et al., 2007; Illera-Vives et al., 2013; Kinnunen et al., 2005; Lema
and Degebassa, 2013; Sahu et al., 2016; Toppe et al., 2018). Fish
and shellfish have a long tradition as fertilizers. In medieval France,
shellfish debris was used along the coast to raise abundant crops
(Wyatt and McGourty, 1990). Fish as fertilizer was used by Egyp-
tians, Incas, and Mayans (Pennington; Plimoth Plantation; Sigma
Marine Products). Fish residues were traditionally used to fertilize
crops in coastal areas. For example, in Nordland county in Norway,
the backbones and heads of cod, and left-over herring were used
directly or after composting to fertilize both leys and row crops
(Helland, 1907, 1908). Around 1880, increasing interest in com-
mercial fertilizers lead to the establishment of several factories
producing ‘‘fish guano” in Norway. Heads of cod and other FW
were steamed or treated with sulfuric acid, dried, ground and
exported, for example to Germany (Helland, 1907, 1908).
Commercial fish-based fertilizers are available for both agricul-
tural and horticultural crops, but not commonly applied in North-
ern Europe, at least not in organic*1 agriculture where one may
expect a relatively more interest in such fertilizers (Løes et al.,
2018). These fertilizers are available in many formulations, such as
meal, bone meal, liquid fertilizer, and compost, possibly also mixed
with seaweeds. As updated on 25 January 2020, 157 fish-
based fertilizers were listed by the Organic Materials Review
Institute (OMRI), and allowed for use in organic* agriculture
(OMRI, 2019b, 2020b), as discussed in Sections 5.1 and 5.2. The
broad availability of commercial fish-fertilizer products indicates
that this is a profitable industry.
1
To distinguish whether the term ‘‘organic” refers to certified organic production,
its inputs and products, or to organic (i.e. carbon-based) materials per se, certified
organic products and production are assigned by an (*).
 I. Ahuja et al. / Waste Management 115 (2020) 95–112
In this review, we present an overview of knowledge, that will
be useful for increasing the utilization of FW as fertilizers. We
focus our research on the applicability of such fertilizers in
organic* farming, and hence, this review deals mainly with FW
from captured fish, and not from aquaculture. Fish raised in aqua-
culture are usually not certified organic*, and the aquaculture
industry has developed quite advanced utilization of FW.
The paper is organized as follows: Section 2 briefs about funda-
mentals of organic* farming systems, recycling of nutrients, and
circular economy. Section 3 explains the nutritional composition
of different species of fish, various fish parts, and some kinds of
FW. Section 4 shows how various FW materials are/can be pro-
cessed to produce different kinds of fertilizers, including digestates
from biogas production. Section 5 lists currently available com-
mercial fish-based fertilizers allowed by the OMRI, while briefly
presenting OMRI’s organic standards and the OMRI Canada pro-
gram. Section 6 discusses the effect on plant growth from applica-
tion of some of the commercial fish-based fertilizers on plants.
Section 7 reviews some studies about production of fish-based fer-
tilizers and their growth effects on a diverse range of plants.
Finally, Section 8 presents the current utilization of FW in Norway
and the potentials for increasing the volumes of FW available for
fertilizer production. Throughout this article, our emphasis is on
the utilization of FW to produce FW-based fertilizers applicable
in organic* farming, and to recycle nutrients from sea to land by
this practice.
2. Organic* farming, nutrients recycling and circular economy
According to the US Department of Agriculture (USDA), organic*
farming production are based on the use of biological, cultural, and
mechanical practices, to promote the cycling of on-farm resources,
maintain ecological balance, and conserve biodiversity. Some of
the examples of such practices are maintaining or enhancing soil
and water quality, and excluding use of synthetic fertilizers, pesti-
cides, growth regulators and livestock feed additives, sewage
sludge, and genetic engineering (Litterick and Watson, 2003;
USDA, 2015). In organic* farming, the fertilization inputs should
be derived from natural substances, preferably from organic* pro-
duction or wild collection (Reganold and Wachter, 2016). Organic*
farming can vary from open systems, which follow organic* certi-
fication guidelines to strict closed-cycle systems that go beyond
organic* certification guidelines by limiting external inputs as
much as possible. To the best possible levels, the organic* systems
rely on off-farm organic* wastes, crop residues, crop rotations, ani-
mal manures, and biological control of pests to maintain soil pro-
ductivity (Reganold and Wachter, 2016).
In Norway, the term organic* is protected through the public
regulations for organic* production, pursuant to the agreement
on the European Economic Area (EEA) (Ministry of Agriculture
and Food, 2018). Hence, the regulations for organic* production
in the EU also regulate this type of production in Norway. Follow-
ing the Annex 1 (European Commission, 2016; Løes and Adler,
2019), the Norwegian Food Safety Authority has defined sediments
from hydrolysed fish (Norwegian: ‘‘grakse”) as fish meal
(Norwegian Food Safety Authority, 2020). Fish meal has been
approved as a fertilizer in organic* farming since the first public
regulations were published by the EU in 1991 (IFOAM Organics
Europe, 2020). Since many of the fertilizers, applied in organic*
farming are wholly or partly based on various types of organic
materials such as by-products, household waste or sludge from
the food industry, different regulations apply to contents of envi-
ronmental toxins, pathogens, plastic etc., in addition to the
organic* regulations. An organic* fertilizer should declare its nutri-
ents, for instance, as nitrogen (N), phosphorous (P), and potassium
97
(K) by their chemical symbols in the order N-P-K or magnesium
(Mg), calcium (Ca), sulphur (S) or sodium (Na), by their chemical
symbols in the order Mg-Ca-S-Na (European Commission, 2016).
The Norwegian Food Safety Authority has delegated executive
control to Debio (the national certification body in Norway), which
carries out an annual review of all organic* production and also
provides important information about organic* production.
(Ministry of Agriculture and Food, 2018; Norwegian Food Safety
Authority, 2012). Farmers and companies wishing to produce, pro-
cess and market organic* food must be approved by Debio. As a
service for farmers and producers of fertilizers, Debio maintains a
database of fertilizers and soil amendments that can be used in
organic* farming (Debio, 2020). The producers are responsible for
the given information and for checking that their products comply
with regulations for organic* farming. Until 16 April 2020, the 125
products listed on Debio’s website did not include any product
from fish or FW. Through personal communication with Debio
(Lene Nilssen, 16 April 2020), it was explained that Debio is some-
times asked whether products made from fish sludge (faeces) or
dead fish from aquaculture can be listed. However, fish sludge is
not permitted as a fertilizer in organic* farming. Moreover, the
silage of dead fish usually contains formic acid, which is not
approved as an input to fertilizers used in organic* farming.
Organic* farming systems are based on recycling of nutrients
through organic* inputs to sustain the fertility of soil–plant sys-
tems and maintain a balance between food production and envi-
ronment preservation (Illera-Vives et al., 2013; Luke Natural
Resources Institute Finland, 2020). Phosphorous (P) has been listed
as one of the crucial raw materials for the EU (Akram et al., 2019;
European Commission, 2017a). This indicates that there is need to
develop new management strategies for this essential plant nutri-
ent mineral, and thereby in the food system. Together with other
nutrients, P is lost from the agricultural soil, or deliberately trans-
ported into the sea as a part of the societal infrastructure (sewage).
Hence, fertilizers derived from the sea and used on field-grown
crops implies the recycling of terrestrial nutrients. Sustainable har-
vesting of natural resources complies well with the principles of
organic* farming, for instance, the basic principle of ecology.
According to International Federation of Organic Agriculture Move-
ments (IFOAM), the principle of ecology states that Organic* Agri-
culture should be based on living ecological systems and cycles,
work with them, emulate them and help sustain them (IFOAM
Organics International, 2020).
Recycling of nutrients is an integrated part of the increasingly
popular circular economy, for instance in the EU, which aims to
limit or avoid the production of waste through reutilization of sec-
ondary raw materials (European Commission, 2015; Greggio et al.,
2018; McDowall et al., 2017). The EU action plan for the circular
(Blue) economy includes policies for waste management, such as
legislative proposals on waste and landfills, proposed changes to
extended produce, remanufacture, or recycling (European
Commission, 2015, 2017b, 2018; McDowall et al., 2017). This pol-
icy fits well with better utilization of residual organic materials, for
instance, as fertilizers. In this context, fish products have relevance
since they can recycle P, a scarce resource, from the sea and back to
terrestrial environments. Reducing waste and pollution by recy-
cling and through efficient exploitation of renewable resources is
the general interest of organic* farming and agrees very well with
the concept of a circular and bioeconomy (Løes and Adler, 2019).
3. Nutrients in fish and FWs suitable as crop fertilizers
Crop plants contain about 30 g of minerals per kg of fresh plant
material (Mengel and Kirkby, 2001). Six macronutrients [nitrogen
(N), phosphorous (P), potassium (K), calcium (Ca), magnesium
98 I. Ahuja et al. / Waste Management 115 (2020) 95–112

(Mg), and sulphur (S)] constitute a significant part of this amount.
Fertile soils may deliver a substantial portion of these elements;
however, most soils are dependent on regular input of fertilizers
containing all macronutrients, and preferably also thirteen
micronutrients required for successful growth.
Fish-based fertilizers usually contain significant amounts of N,
P, and Ca as compared to the demands for these nutrients by crop
plants (Dominy et al., 2014; Fahlivi, 2018; Illera-Vives et al., 2015b;
Kazemi et al., 2017). Such fertilizers commonly also contain S, but
are less well balanced concerning the needs of crop plants for the
macronutrients K and Mg.
The billion-dollar mineral N fertilizer industry shows the signif-
icance of N as one of the main elements of crop production (Rütting
et al., 2018). P is another vital macronutrient required for agricul-
ture and food production. More than 85% of P applied in agriculture
comes from phosphate rock, which is a limited resource (Cordell
and White, 2011; Nedelciu et al., 2019). Soil characteristics affect
the availability of P to crop plants, and Lateritic soil, for example,
commonly found in tropical regions, has a very high binding capac-
ity for phosphate, restricting P availability. In calcareous and alka-
line soil, high pH limits the plant availability of P. Hence, fertilizers
rich in P may have a broad range of applications.
Fish bones are comprised of 60–70% minerals, which mainly
include Ca and P as hydroxyapatite (Ca10(PO4)6(OH)2) (Ghaly
et al., 2013; Kim and Mendis, 2006). Fish scales are also rich in
nutrients, especially N. Additionally, fish scales contain P and Ca
since they are composed of a layer of hydroxyapatite and calcium
carbonate surrounding a kernel of collagen, which is a protein
(Basu and Banik, 2005; Harikrishna et al., 2017). In a study aimed
at describing the risk of accumulating radioactive minerals in sea-
food (Goldberg, 1962), elemental composition analysis of tissues
from some pelagic fish species showed that depending on the
organ, Ca, P, K, Mg, sodium (Na), silicon (Si), and aluminium (Al)
were the most common elements. However, N contents were not
analysed in that study.
The contents of the macronutrients, N, P, K, and Ca from differ-
ent fish species, as analysed and reported by (Bogard et al., 2015;
Palani et al., 2014), are shown in Table 1. The average values of
N-P-K for fish from inland capture were 120:11:13, and from mar-
ine capture, these were 130:16:11 (Bogard et al., 2015). From mar-
ine capture, the average contents of Ca were 21.0 g per kg DM
(Table 1). The nutritional composition between species can vary
with fish size and with the inclusion/exclusion of tissues like head,
bones, and also viscera (Bogard et al., 2015). Average Ca contents in
edible fish parts were observed to be 31 g per kg DM (Palani et al.,
2014). The average N contents were almost the same in both stud-
ies (12–13% of DM) (Bogard et al., 2015; Palani et al., 2014).
In a study of bones from cod heads, subsequent to pilot-scale
hydrolysis to remove muscle tissue (Ahuja and Løes, 2019), a high
concentration of Ca (300 g per kg DM), and P (120 g per kg DM) was
confirmed (Table 2). In another Norwegian study, bones from var-
ious fish species (Table 2) were separated from other parts follow-
ing different processing steps, and then freeze-dried (Toppe et al.,
2007). The N contents in fish bones ranged between 4 and 7% of
DM, P contents from 90 to 123 g per kg DM, Ca contents from
140 to 239 g per kg DM, and Mg contents from about 2 to 4 g
per kg DM.
Fish powder obtained from the processing of dried tuna- frames
and gills (Abbey et al 2017) showed high calcium contents as com-
pared with powder from trimmings; 144, and 166 g per kg DM for
frames and gills, respectively, compared to 11.2 g per kg DM for
trimmings (Table 2). Also, for P, the content was close to twice as

Table 1
Contents of macronutrients N, P, K, and Ca in various fish species following analyses using different methods.

Fish species analysed after exclusion of non-edible parts/fish beheaded, gutted, washed and N (*) % P K Ca
filleted prior to analysis of DM or air-dried g/kg DM g/kg DM g/kg DM
material
Inland Capture - Large fish species (Bogard et al., 2015)

Gojar (Channa marulius) and Shol (Channa striatus): (bones, viscera, fins, scales, and gills excluded prior to analysis)

Ilish (Tenualosa ilisha) and Jatka Ilish (T. ilisha) (juvenile): (bones, viscera, fins, and scales excluded prior to analysis)

Mean and (S.D.) for N, P, K and Ca (n = 4) 12.2 (4) 10.6 (3) 13.2 (6) 7.2 (7)
Marine capture (Bogard et al., 2015)

Foli Chanda (Pampus argenteus): (bones, viscera, and fins excluded prior to analysis)

Maita (Scomberomorus guttatus), Murbaila (Platycephalus indicus), Tailla (Eleutheronema tetradactylum), and Tular Dandi (Sillaginopsis panijus): (bones, viscera, fins
and scales excluded prior to analysis)

Parse (Liza parsia): (bones, viscera, fins, scales and gills excluded prior to analysis)

Kata Phasa (Stolephorus tri) (viscera excluded prior to analysis)

Lal Poa (Johnius argentatus) (viscera, fins, and scales excluded prior to analysis)

Mean and (S.D.) for N, P, K and Ca (n = 8) 13.2 (3) 16.2 (14) 10.5 (4) 21.0 (31)

Medium sized marine finfishes: (Fish were beheaded, gutted, washed and filleted prior to analysis)
(Palani et al., 2014)

Rainbow sardine (Dussumieria acuta), Ilisha melanostoma, Indian pellona (Pellona ditchela), Indian oil sardine (Sardinella longiceps), Fringescale sardinella (Sardinella
fimbriata), Yellowstripe scad (Selaroides leptolepis), Dorab wolf-herring (Chirocentrus dorab), Commerson’s anchovy (Stolephorus commersonii), Devis’ anchovy
(Stolephorous devisi), Thalassoma fuscum, Leiognathus dussumieri, Smalltoothed ponyfish (Gazza achlamys), Lethrinus lensus, Five-lined snapper (Lutjanusquinquelin-
eatus), Bigeye snapper (Lutjanus lutjanus), Checkered snapper (Lutjanus decussatus), Nemipterus bleekeri, Nemipterus japonicus, Scolopsis bimaculatus, Indian mackerel
(Rastrelliger kanagurta), Areolate grouper (Epinephelus areolatus), Obtuse barracuda (Sphyraena obtusata), and Greater lizardfish (Saurida tumbil)

Mean and (S.D.) for N, P, K and Ca (n = 23) 11.7 (2) 2.2 (1) – 31.3 (19)
*
Nitrogen amount was calculated from proteins by dividing with 6.25 (Kjeldahl factor).
 I. Ahuja et al. / Waste Management 115 (2020) 95–112 99

Table 2
Composition of macronutrients: N, P, K, Ca, and Mg in bones from various fish species, and the powder obtained from trimmings, gills, and frames of tuna.

FW: hydrolysed fish bones, N P K Ca Mg

(% of DM or (g/kg DM) (g/kg DM) (g/kg DM) (g/kg DM)
air-dried material)
Bones of heads from cod (Gadus morhua) subsequent to hydrolysis (Ahuja and Løes, 2019)
Dried fish bones 5.04 120 1.7 300 3.8
Fish bones from various white fish and pelagic species (N*) (Toppe et al., 2007)
Cod 6.21 123 0.006 206 3.3
Blue whiting (Micromesistius poutassou) 7.15 93 0.003 181 3.4
Salmon (S. salar) 4.92 85 0.009 142 2.3
Trout (Salmo trutta) 5.31 92 0.008 155 2.5
Herring 1 (small) (Clupea harengus) 6.43 101 0.005 173 2.8
Herring 2 (large) (C. harengus) 5.02 99 0.008 205 3.0
Mackerel (Scomber scombrus) 4.37 90 0.007 150 2.7
Horse mackerel (Trachurus trachurus) 4.44 114 0.005 239 3.7
Mean and (S.D.) for N, P, K, Mg and Ca (n = 8) 5.5 (1) 100 (13) 0.006 (0.002) 182 (34) 3.0 (0.5)
Fish powder from dried tuna-trimmings, frames, and gills (Abbey et al., 2017)
Tuna trimmings 13.56 6.31 – 11.20 –
Tuna frames 5.01 11.03 – 143.93 –
Tuna gills 6.57 11.50 – 165.98 –
*
Nitrogen amount was calculated from proteins by dividing with 6.25 (Kjeldahl factor).

high in powder from frames and gills (Table 2). For N, the powder
from trimmings had almost twice as high contents of total N, 14%
of DM than powder from frames and gills, 5–7% of DM (Table 2). A
study comparing incinerated waste bones from fish and chicken for
struvite precipitation found that fish bones had somewhat higher
concentrations of P and Ca (170 and 221 g per kg DM, respectively)
than chicken bones (155 and 210 g per kg DM, respectively)
(Darwish et al., 2017). The analysis of fish scales from five different
fish species showed N to vary from about 5 to 11% (Harikrishna
et al., 2017). A recent study analysed P and Ca contents from pro-
cessed by-products, such as fish bones, gills, guts, muscles, and
skin of gilthead sea bream (Sparus aurata) (Pateiro et al., 2020).
The contents of P ranged from 1.8 to 13 g per kg, where fish bones
showed about 10 and heads 13 g per kg. However, the data were
not presented as per g DM (Pateiro et al., 2020). Heads and fish
bones also showed high Ca contents, from 16 to about 24 g per
kg. The K contents were generally low in fish bones and other
FW, ranging from 0.003 to 1.7 g per kg DM (Table 2) in comparison
to the processed fish, (10.5 and 13.2 g per kg DM, respectively)
(Table 1).
The referred studies show that fish/FW possess substantial
amounts of minerals, which may play a significant role in meeting
the nutritional requirements of crop plants.
4. Processing of fish/FW for use as feed or fertilizer
Fish/FW can be processed into stabilized liquid or solid forms of
fertilizers and be combined with other materials to produce fish
compost (Fig. 1A and B) or applied as a substrate in anaerobic
digestion (Table S2), which has been discussed later in this section.
Depending upon the method of processing, several terms are
used to describe FW products, including fish solubles/fish emul-
sion, fish soluble nutrients, hydrolysed waste/fish hydrolysate (also
called fish silage), fish meal, and fish powder. Processing steps vary
according to the type of material and can include grinding, heating,
pressing or centrifugation, separation into solid and liquid phases,
drying of solid materials and grinding of dried materials to the
desired particle size (FAO, 1986; Remme et al., 2018; USDA,
2019a). Heating coagulates proteins, ruptures fat depots, and liber-
ates oil and physiochemically bound water. The liquid phase is sep-
arated into oil and stick water (solubles), and the solid phase is
used to create meal. Fish meal is usually produced through heating,
pressing, separation, evaporation, drying, and grinding (Ghaly
et al., 2013; Shaviklo, 2015). For drying, different techniques, like
freeze-drying, spray drying, and oven-drying, are applied. Besides,
fish meal can also be produced through fermentation (Yamamoto
et al., 2005).
The fish hydrolysate or fish silage can be further dried/modified
into fish meal, fish bone meal or fish powder, and used in animal
and feed, apply as fertilizers or mixed with other materials to cre-
ate fish compost (Arvanitoyannis and Kassaveti, 2008; Dominy
et al., 2014; Fagbenro and Jauncey, 1994; FAO, 1986; Goddard
and Perret, 2005; Ihemanma and Ebutex, 2013; Palkar et al.,
2018; Sahu et al., 2016; Toppe et al., 2018). Fish meal or fish bone
meal can be used in solid and liquid fertilizer products. For the lat-
ter, the meal should be finely grinded to remain in suspension and
flow through dispersion nozzles when dispensed through sprayers
(Dominy et al., 2014; Wyatt and McGourty, 1990). The production
of fish emulsion, fish hydrolysate, and fish compost by adapting
different processes is shown in Fig. 1B and also detailed below.
4.1. Fish emulsion
Fish emulsion is produced by heating FW at temperatures of
>80 °C to extract oils and kill most of the putrefaction bacteria
(Beckley et al., 2007; Parker, 2015; USDA, 2006). The solid material
is pressed into a cake, which can be dried to produce fish meal. The
fish emulsion is the liquid residue that has been pressed out of the
fish cake (Fig. 1B). Liquid residue contains mainly water-soluble
nutrients and moderate or low amount of oil-soluble nutrients
(Beckley et al., 2007). Fish emulsion may be acidified with sulfuric,
phosphoric or organic acids to stabilize it (Abbasi, 2011; USDA,
2006).
4.2. Fish hydrolysate (fish silage)
Fish hydrolysate, also called fish silage, is produced using differ-
ent methods (Fig. 1B). These include the liquification through
endogenous enzymes, or by adding enzymes and then stopping
the process by adding acids, or by using fermenting agents
(Beckley et al., 2007; Knuckey et al., 2004; Parker, 2015; USDA,
2006). Scientists have used either fish hydrolysate or fish silage
depending on the method they have used. If the fish silage is pro-
duced by adding acids, then it is called acid silage, and if produced
through fermenting agents, then it is termed fermented silage. The
processes of fish hydrolysis; especially the hydrolysis of fish bones,
and methods to produce acid silage and fermented fish silage, are
discussed below.
100 I. Ahuja et al. / Waste Management 115 (2020) 95–112
Fig. 1. A. Flowchart showing how FW can be processed to produce dry fertilizers,
liquid fertilizers, and fish compost. Dry fertilizers can be further converted to
produce liquid fertilizers or mixed with bulking agents and other amendments to
produce fish compost. B. Flowchart showing different methods to produce fish
emulsion, fish hydrolysate/fish silage, and fish compost.
4.2.1. Fish hydrolysate(s) through enzymes
Fish hydrolysate(s) are produced by applying different hydroly-
sis methods (Ghaly et al., 2013; USDA, 2006). Hydrolysis can be
carried out by mincing the whole fish, or FW, acidifying, thor-
oughly mixing, and liquefaction. Liquefaction is an autolytic
method that is carried out by endogenous enzymes and acceler-
ated by the application of acids, which induces the proper condi-
tions for the enzymes to breakdown the tissues and limits the
growth of spoilage bacteria (Anon., 1987; Beckley et al., 2007;
Gildberg, 1993; USDA, 2006). The hydrolysis process starts when
endogenous enzymes in the fish are released from the cells and
digest the fish tissue. The mixture may be stirred or agitated until
the completion of enzymatic hydrolysis (Beckley et al., 2007;
Knuckey et al., 2004). The mixture is adjusted to be acidic, with
range from pH 1.0 to pH 4.0, where pH 2.0–3.0 is preferred
(Beckley et al., 2007). Within range of pH 3.0–3.5 pH, the liquid fish
products and the hydrolysed fish can be stored for quite long peri-
ods (Knuckey et al., 2004). A variety of acids, such as hydrochloric,
sulfuric, phosphoric, formic, or propionic acid, can be used individ-
ually or in combination (Arruda et al., 2006; Beckley et al., 2007;
Ghaly et al., 2013; Knuckey et al., 2004; Norouzi, 2013; Toppe
et al., 2018). An example method for production of fish-based fer-
tilizers, with US patent no. US20070261451A1, has been described
by Beckley and co-workers (Beckley et al., 2007). This method
includes blending the whole fish or FW with water, mechanically
reducing the particle size, acidifying the fish-water mixture by
addition of phosphoric acid, hydrolysing under ambient conditions,
and then filtering and collecting the filtrate to be used as a soil
additive or fertilizer. Alternatively, the filtrate may be used for
feed, and the residual sediments for fertilization.
After removal of fish oil and liquefied proteins from storage
tanks of fish hydrolysate, sediments of grinded fish are usually dis-
posed of as waste or used for biogas production (Remme et al.,
2018). These sediments of hydrolysed FW contain significant
amounts of fish bones. Another study described that after mincing
of backbones and separation of the oil fraction, the mixture of stick
water and sediments could be used as a raw material for hydrolysis
(Slizyte et al., 2016). The process of hydrolysis can be started by
adding an enzyme(s) when the temperature of the mixture of the
raw material has reached 50 °C, followed by enzyme inactivation
using microwave heating at temperature >90 °C.
4.2.2. Acid fish silage
Acid fish silage is a liquid product made from whole fish or
minced fish by-products. It is liquified by the action of endogenous
enzymes in the presence of added organic or inorganic acids (‘‘acid-
preserved silage”) (Anon., 1987; Dominy et al., 2014; FAO, 2001; Raa
et al., 1982; Toppe et al., 2018). The acid silage method was devel-
oped in Finland in 1920 by A. I. Virtanen, using hydrochloric and
sulfuric acid for the conservation of forages (Anon., 1987; Arason,
1994; Tatterson and Windsor, 1974). In 1936, Edin adapted this
method to preserve and liquify different types of fish and fish
waste (Edin, 1940). Production of fish silage on the industrial scale
started in 1948 in Denmark. In 1974, a large-scale research pro-
gram was launched by Norwegian scientists to produce fish silage
from fish viscera and offal. Fish silage processing became increas-
ingly popular in Norway along with the rapid growth of aquacul-
ture, enabling oils and protein from fish silage to replace fish
meal and oil from captured fish (Anon., 1987).
Acid preservation is a simple technique to preserve processed
fish by-products (Olsen and Toppe, 2017). The amount of acid that
is necessary depends on the raw material, and usually, formic acid
is used. Formic acid is often more expensive than mineral acids;
however, such silage does not need to be neutralized before being
used for feed (Arruda et al., 2007; Ramasubburayan et al., 2013).
The stable liquid that is produced has a malty odour and good stor-
age characteristics, although, the quality depends on the freshness
of the raw material (Arason, 1994; Toppe et al., 2018). Lipid oxida-
tion can be prevented by adding antioxidants, such as ethoxyquin
or butylated hydroxytoluene (BHT). However, ethoxyquin was
recently suspended as a feed additive for all animal species and
categories in EU countries (EUR-Lex, 2017). Liquid fish silage can
be combined directly into moist feeding diets, condensed, or dried
to be used as an ingredient of animal feed or as fertilizer (Goddard
and Perret, 2005). Acid preserved fish silage is almost sterile, does
not putrefy, and maintains a fresh acidic smell even after storage
for weeks at tropical temperatures (Dominy et al., 2014).
Several studies have detailed the production of acid fish silage
from diverse kinds of fish species/FW with some variations in
methods (Table 3). These include using various acids (mineral/or-
ganic or a mixture of both), different temperatures during liquifica-
tion, stirring techniques, different numbers of days for
 I. Ahuja et al. / Waste Management 115 (2020) 95–112 101

Table 3
Acids, temperatures, and days used in the preparation of acid fish silage.

Acid fish silage

Fish/FW Acids Temperature and days for Country Reference
(preparation/liquification/
incubation/preservation/storage)
Short-bodied Formic acid (3%) * 30 °C, 60–180 days Indonesia (Hasan, 2003)
mackerel (Rastreliger brachysoma)
FW (heads and entrails) Formic acid (3%) * 30 °C, 40 days Indonesia (Kristanto and Riyadi,
of tuna 2018)
(Aurius thazard)
FW Sulphuric acid 25–28 °C, 15 days India (Pagarkar et al., 2006)
(3–4%) (w/v), Formic
acid and
propionic acid, (both
1.5–2%; 1:1 ratio) (w/w)
Nile tilapia Acid mixture (3%) 27 °C, 3 days Brazil (Arruda et al., 2006)
(Oreochromis niloticus) Propionic and formic; of
1:1) (v/w)
Indian oil sardines, (Sardinella longiceps) 1.5% acid mixture 34–44 °C, 2 days Sultanate (Goddard and Al-
(propionic and formic of Oman Yahyai, 2001;
acid; 1:1) (v/w) Goddard and Perret,
2005)
Long-tail tuna Sulphuric acid (2.5, 3.5 28–32 °C, 76 days Iran (Mousavi et al., 2013)
(Thunnus tonggol), Kawakawa and 4.5%)
(Euthunnus afinis) Formic acid (2.5, 3.5 and
Skipjack tuna (Kasuwonus pelamis) 4.5%) (w/w)
Sardine (S. fimbriata, S. longiceps), Mackerel (Rastrelliger Sulphuric acid 28–32 °C, 60 days India (Palkar et al., 2017)
kanagurta), Tuna (Euthynnus affinis, Auxis thazard), (2.5, 3.5 and 4.5%) following the methods
Pink perch (Nemipterus japonicus), Ribbon fish (Trichiurus (v/w) by
lepturus, Lepturocanthus savala), Bombay duck (Harpadon (Mousavi et al., 2013)
nehereus), Seer fish (Scomberomorus guttatus, S. commerson),
Mullet (Mugil cephalus) Formic acid
(2.5, 3.5 and 4.5%)
(v/w)

FW from Rui (Labeo rohita), Catla (Labeo catla), Mrigal Formic acid 25–30 °C, 2–5 days, and 20– Bangladesh (Hossain and Alam,
(Cirrhinus cirrhosis), Tilapia and Pangas (Pangasias) (2, 3 and 4 and 5%) * 30 °C, 4 months (storage) 2015)

*
v/w or w/w not mentioned.

liquification/preservation/preparation, and with/without antioxi-
dants (Anon., 1987; Arason, 1994; Goddard and Al-Yahyai, 2001;
Mousavi et al., 2013; Olsen and Toppe, 2017; Toppe et al., 2018;
Vidotti et al., 2003).
4.2.3 Fish silage through bacterial fermentation and
microorganisms
Fermented fish silage has been traditionally produced through
bacterial fermentation using Lactobacilli starter culture. A starting
culture of lactic acid bacteria, for example, Lactobacillus plantarum,
may rapidly convert sugars to acids, which preserves the whole
mass (Anon., 1987; Dominy et al., 2014; Olsen and Toppe, 2017;
Raa et al., 1982; USDA, 2006). Since FW often contains low
amounts of carbohydrates, fermentable sugar such as molasses or
fruit processing waste may be added to obtain a stable silage with
a pH of around 4.0. A culture of lactic acid bacteria may be inocu-
lated into molasses and incubated until a population of 107 bacte-
ria per g molasses is obtained, and this culture can then be added
to the minced fish (Ghaly et al., 2013). Such fermentation is more
easily achieved in regions with high and stable ambient tempera-
tures. Fermented fish silage has been prepared from different kinds
of fish species/FW by adapting different processes, with variations
in the use of fermenting agents, source of carbohydrates, starter
cultures, temperatures, and days to prepare, and some examples
are shown in Table 4.
4.3. Fish compost
Composting is an aerobic (oxygen requiring) biological decom-
position of organic matter into a stable, humus-like product
(Archer et al., 2001; Rynk et al., 1992). During the process, the
organic matter is decomposed by microorganisms. It is essentially
the same process as natural decomposition except that it is
enhanced and accelerated by mixing organic waste with other
ingredients to optimize microbial growth (USDA, 2000). However,
the temperature increase and rapid decomposition, integrated
into a successful composting process, imply a risk of losing signif-
icant amounts of valuable plant nutrients, primarily N and S, by
gas emissions (Løes et al., 2020). Composting of FW is an effective
way to reduce the volume of waste FW, and compost enriched
with FW may be a good organic* fertilizer (Illera-Vives et al.,
2013; Kazemi et al., 2017; Laos et al., 1998; Liao et al., 1997;
Radziemska et al., 2018). The composting process of FW is based
on the addition of bulking agents to facilitate aeration through
the pile and provide carbon sources for microorganisms. For suc-
cessful composting, factors such as pH, moisture, bulk density,
and carbon to nitrogen (C:N) ratio need monitoring. The optimal
C:N ratio of the total substrate in compost should be about 20–30
(Archer et al., 2001; Batham et al., 2013; Busato et al., 2018;
Illera-Vives et al., 2017; Liao et al., 1997; Liao et al., 1995b). Fish
may be a useful substrate to decrease the C:N ratio towards 20–
30, which is favourable for composting when treating waste
materials rich in C. Various bulking agents, such as sawdust,
wood shavings, bark, crop residues, rice hulls, leaves, crushed
grass, wheat bran, and straw have been mixed with FW to pro-
duce FW-based compost (Table 5). Besides, other amendments
like seaweeds, poultry litter, and peat have also been mixed to
FW (Busato et al., 2018; Kazemi et al., 2017; López-Mosquera
et al., 2011).
102 I. Ahuja et al. / Waste Management 115 (2020) 95–112

Table 4
Fermenting agents, starter cultures, temperatures, and days to the preparation of fermented fish silages/other similar kinds of liquid fertilizers.

Fish/FW Fermenting agents and Temperature and days for Country Reference
carbohydrate source preparation/fermentation/
liquification/incubation/
preservation
Tilapias (Orechromis spp.) L. plantarum and 30 °C, 7 days UK (Fagbenro and Jauncey, 1994; Fagbenro
Tread fin seabream, Nemipterus japonicus sugarbeet molasses and Jauncey, 1995)
Temperature*, days* (Karim et al., 2015) following (Fagbenro
L. acidophilus and Malaysia and Jauncey, 1995)
molasses

Sardina pilchardus L. plantarum and molasses 22 °C, 20 days Morocco (Hammoumi et al., 1998)

Short-bodied L. pentosus and molasses Indonesia (Hasan, 2003)

mackerel (Rastreliger brachysoma) L. plantarum and molasses 30 °C, 60 days

FW L. plantarum and molasses Room temperature, 15 days India (Pagarkar et al., 2006)

Shrimp by catch, Mexican barracuds wastes, and L. plantarum and 30 °C, 10 days (240 h) Mexico (Ramírez-Ramírez et al., 2008,; Ramírez-
Mixtures of FWs; Mixtures of waste: Bagre Lactobacillus sp. B2 Ramírez et al., 2013
panamensis, salema butterfish (Peprilus (isolated from shrimp
snyderi), wastes), and sugar cane
Mexican barracuda (Sphyraena ensis), derbio molasses
(Trachynotus ovatus), meagre (Argyrosomus
regius) and common two-banded seabream
(Diplodus vulgaris)
Long-tail tuna, Kawakawa and Skipjack tuna L. plantarum and Temperature*, 20 days Iran (Mousavi et al., 2013)
fermentable sugar from
sugar beet pulp
FW (head protion, intestines and gills) Jaggery (unrefined sugar) 14 days India (Balraj et al., 2014) (Hepsibha and
Geetha, 2017), prepared following the
method described by (Vincent et al.,
2014)
Tilapia fish/FW Sugarcane molasses/ 37 °C for 28 days India (Sahu et al., 2014)
Jaggery
FW from Tuna L. plantarum and molasses 30 °C, 40 days Indonesia (Kristanto and Riyadi, 2018)
(Aurius thazard)
Sardine, Mackerel, Tuna, Pink perch, Ribbon fish, Curd: a source of lactic Ambient temperature, India (Palkar et al., 2018)
Bombayduck, Seer fish, and Mullet acid bacteria 10–12 days

*
Not mentioned.

The composting time for FW with peat moss in a passively aer-
ated windrow method was 8–10 weeks (Rynk et al., 1992). Peat has
a good ability to reduce gas emissions of N when applied as a sub-
strate or cover of a windrow compost with FW (Martin, 1998;
Mathur, 1991). In a three-bin compost system with FW, the bins
are filled one after the other. When the second bin is full, the first
bin can be turned by shovelling it over into the third bin. Each pile
can be consecutively turned in this manner every several days until
the compost is complete (Carney et al., 2000; Zamudio et al., 2011).
Fish composting systems tried in different studies varied from sim-
ple to complex, following various methods/equipment, such as in-
vessel composting bays, compost- pits and bin-systems, wooden
crates, reactors and ceramic pots (Table 5). The compost produced
with a combination of FW, seaweed and pine bark was considered
to be stable, hygienic, rich in organic matter, and applicable as fer-
tilizer in organic* farming systems (Illera-Vives et al., 2013; López-
Mosquera et al., 2011). Compost produced using FW with crushed
grass showed pH value, C/N ratio, and electrical conductivity that
allowed it to be used as an organic* fertilizer (Busato et al., 2018).
4.4. Anaerobic digestion of FW and possible use of biogas digestate as
fertilizer
Anaerobic digestion (AD) in biogas plants is a well-established
recycling technology that has a substantial potential for managing
biodegradable solid waste. During AD, the organic matter (sub-
strate) breaks down in an oxygen free environment (digesters),
hence producing biogas and digestate (digested substrate) (Ali
et al., 2019; Eiroa et al., 2012; Ivanovs et al., 2018; Lukehurst
et al., 2010). Essential plant nutrients such as N and P are retained
in digestates, and thus digestates from AD comprise beneficial fer-
tilizers/soil amendments (Atelge et al., 2020; Estevez et al., 2014;
Kafle and Kim, 2012; Nges et al., 2012; Serrano et al., 2013). FW
can be of variable nature depending on fish species and processing
and may contain approximately 20% ether extract or fat, about 60%
proteins, and minerals (Ghaly et al., 2013; Ivanovs et al., 2018). In
addition, in FW, there are sufficient amounts of monosaturated
acids, palmitic acid, and oleic acid (22%). Anaerobic co-digestion
of FW with other organic wastes, especially agricultural wastes,
can be considered a valued approach for utilization of FW to gen-
erate energy; thus, playing a significant role in future of biofuels
(Ivanovs et al., 2018; Kafle and Kim, 2012). AD/Anaerobic co-
digestion of FW seems to have emerged more in the 2010s. Some
of the studies (Bermúdez-Penabad et al., 2017; Choe et al., 2020;
Eiroa et al., 2012; Estevez et al., 2014; Hadiyarto et al., 2015;
Kassuwi et al., 2012; Mshandete et al., 2004) that have investigated
anaerobic digestion/co-digestion of FW with other materials are
presented in Table S2. FW has been applied as a substrate in co-
digestion with other materials, such as cow dung, cattle manure,
strawberry exudate, sisal pulp, bamboo residues, and the vegetable
fraction of market solid waste (Choe et al., 2020; Ivanovs et al.,
2018). Anaerobic co-digestion of FW with the liquid fraction of
hydrothermal carbonization of bamboo residues has been pro-
posed as a strategy to manage liquid waste that is complex to
degrade (Choe et al., 2020). The co-digestion of FW with straw-
berry waste yielded a digestate that was rich in nutrients
(Serrano et al., 2013). A patent from the US presented a process
to generate an anaerobic digestate-based fertilizer product, which
 I. Ahuja et al. / Waste Management 115 (2020) 95–112 103

Table 5
Composting processes adapted to produce compost from FW.

FW FW mixed with bulking agents/substrates/ Method adapted; Equipment used and Countries Reference
amendments/others the period during the process of
composing
FW (consisted mainly of fish guts/fish Sawdust with FW (1.3:1) (w/w); FW mixed A receiving tank, a mixing vessel, and Canada (Liao et al., 1997;
viscera) with fir sawdust (1:3) (by weight) and four agitated, in-vessel composting Liao et al.,
added alder chips, peat moss, and bays; composting materials were 1995a)
vermiculite retained in composting bays for
18 days
FW FW with rice hulls, straw and water (1:1.5; Three-bin compost system/ US (Carney et al.,
0.5–0.75: 0.0–0.5) (parts by volume) Constructing pile 2000)
FW (intestines, bones, scales, fins, gills) from FW Compost pits Senegal, (Ndiaye et al.,
(Sardinella orita) (placed into compost pits for 4– US 2000)
6 weeks)
Fish offal Fish offal with a mixture of sawdust + wood 220-litre PVC reactors Argentina, (Laos et al.,
shavings (3:1; by weight) (wood shavings: First mixed then remixed after 20 days, Spain 1998)
native cypress; Austrocedrus chilensis and two periods of composting of about
Douglas-fir (Pseudotsuga menziesii) 100 days at different temperatures

Fish offal Fish offal with a mixture of sawdust + wood Static aerated piles (in-vessel method) Argentina, (Laos et al., 2002)
shavings (3:1; by weight) (wood shavings: in 220-Liter PVC reactors - Spain following
native cypress; and Douglas-fir) first mixed then remixed after 20 days, (Laos et al.,
composting period: 90 -100 days 1998)

FW came from the processing of (mackerel, FW with seaweeds Laminaria sp. and The compost pile was created using the Spain (López-
sardine, tuna, squid) Cystoseira sp.) and pine bark (1:1:3) (by windrow method, Mosquera et al.,
volume) Composting period: 4 months 2011)
FW was derived from horse mackerel FW with seaweeds Laminaria spp. and Windrow method using conical piles Spain (Illera-Vives
Trachurus Cystoseira spp. and pine bark (1:1:3) (by system et al., 2013), fol-
trachurus volume) Composting period: 10 weeks lowing (López-
Mosquera et al.,
2011)
FW (basic substrates: small cyprinid fish Compost 1: fish waste (80% d.m.), sawdust Wooden crates Poland (Radziemska and
from Lake Kortowskie (Olsztyn, Poland): (20% d.m.); Mazur, 2015)
common bleak (Alburnus alburnus), Compost 2: fish waste (80% d.m.), straw
common roach (Rutilus rutilus), common (20% d.m.);
bream (Abra-mis brama) and white bream Compost 3: fish waste (80% d.m.), bark (20%
(Blicca bjoerkna) d.m.);
Compost 4: fish waste (79.3% d.m.),
sawdust (19.7% d.m.), lignite (1% d.m.);
Compost 5: fish waste (79.3% d.m.), straw
(19.7% d.m.); lignite (1% d.m.);
Compost 6: fish waste (79.3% d.m.), bark
(19.7% d.m), lignite (1% d.m)
FW FW (80%) with pine bark (20%) (by weight) - Poland (Radziemska
et al., 2018)
Residues from the filleting of freshwater fish Pine wood shavings mixed with residues of Waterproof composting cell and in a Brazil (Valente et al.,
freshwater fish (3:1) (by mass) pile 2014)
Composting period: 90 days
Marine FW Marine FW with reused pine wood Waterproof composting cell Brazil (Valente et al.,
(skin and fin) shavings (Pinus spp.) (7: 3) (by mass) Composting period: 60 days 2017)
Cod fish wastes Peat with FW (1:10) (by weight) 35 L bench-scale cylindrical reactor, Canada (Kazemi et al.,
(a complex mixture of fish heads, bones, composting by enzyme activities, 2017)
and viscera) Composting period: 60 days
Fish residues from open fairs Fish residues with shavings/grass cutting/ Wooden composters Brazil (Nascimento
pruning of trees Composting period: 40 days et al., 2018)
FW from tilápia (Oreochromis niloticus) FW with crushed grass (Pennisetum 40-L ceramic pots Brazil (Busato et al.,
beneficiation purpureum) (3:1) (by weight; dry base) Composting period: 120 days, ceramic 2018)
pots being turned over weekly during
the first 45 days

includes combining and processing anaerobic digestates with sta-
bilized liquid fish products (Evans, 2017).
5. The OMRI, OMRI-allowed fish-based fertilizers products, and
applicability
5.1. About OMRI, and the OMRI’s Canada program
The Organic Materials Review Institute (OMRI) is a non-profit
organization creating trust and integrity in the organic* sector.
OMRI reviews various products for their suitability for use in
organic* production and provides a platform for listing accepted
products on their website https://www.omri.org/. Fertilizers, pest
controls, and livestock care products that comply with organic
standards are ‘‘OMRI ListedÒ”. The ‘‘OMRI ListedÒ” products follow
the USDA National Organic Program (NOP) (USDA, 2019b), while
products listed under OMRI Canada Products List follow Canada
Organic Regime (COR) (OMRI, 2020a,b). Producers can use these
listings to determine products that can be used in organic produc-
tion https://www.omri.org/. The COR is a non-traditional regime for
the Canadian Food Inspection Agency (CFIA) (Canadian Food
Inspection Agency, 2019a,b; OMRI, 2019a).
In the US, the term ‘‘organic” is currently not regulated for many
non-food products such as pet food, household products, and fertiliz-
ers. For instance, ‘‘OMRI Listed,” fertilizer may mean that it meets
OMRI’s standards for fertilizer, but almost any fertilizer can use
104 I. Ahuja et al. / Waste Management 115 (2020) 95–112

the term ‘‘organic” on the label. The Canadian laws are also similar investigated in scientific research (Table 6). The referred studies
in this respect (OMRI, 2019d). The fish-based fertilizers in OMRI- were performed with commercially available fish-based fertilizers,
listed products are produced from different sources, for instance, such as fish- meal, fish-scale meal, fish pellets, fish-derived protein
FW that is available after processing of market fish, fish by catch hydrolysates, hydrolysed fish extracts, fish emulsion, and fish bone
and mortality (caught or damaged unintentionally while harvest- formulations. Significant results related to growth effects on agri-
ing fish for non-fertilizer use), fish harvested for wet reduction pro- cultural and horticultural plants, tree species, and berries (Table 6)
cessing (meal, oil, and solubles) or combinations (FW + bycatch are described below.
and mortalities/ fish waste + meal, oil, and solubles) (OMRI, Agro fish pellet positively affected the growth parameters of
2019c; USDA, 2019a). tomato plants, through an increase in stem diameter, shoot dry
weight, number of flowers and fruits, fruit yield, and overall fruit
quality (Kalbani et al., 2016). Fish meal and fish-scale meal after
5.2. Commercially available fish-based fertilizers listed by OMRI
mixing with a peat-compost growing medium, enhanced the
shoot-weight of greenhouse tomato transplants (Gagnon and
A lot of fish-based fertilizers, single-source as well as blended
Berrouard, 1994). Fish bone meal, by itself, or in combination with
products, are commercially available from different suppliers and
marine sediments, or seaweed + fish oil was applied over six grow-
distributors, as per the information gathered from https://www.
ing seasons to a 3-year vegetable crop rotation composed of cab-
omri.org/omri-lists (Tables S3 and S4) (OMRI, 2019b, 2020a,b),
bage, carrot, and green beans. Attained marketable yields of
and as previously discussed (Gaskell and Smith, 2007). The fertiliz-
cabbage and carrots were comparable with yields obtained by
ers are available with different concentrations of nutrients (N-P-K)
standard vegetable mineral fertilizer (NPK: 17–17–17), whereas
(Tables S3 and S4), as indicated in the name of products. For exam-
yields of beans were better with mineral fertilizer (Blatt and
ple, Brown’s Fish Hydrolysate Liquid Fertilizer 2-3-1, Down to Earth
McRae, 1998).
All Natural Fertilizer Fish Meal 8-6-0 (Table S3), and Pacific NaturalÒ
HFPC hydrolysed powder supported colonization of leek roots by
Fresh Fish Fertilizer 2-3-0 and Purely Fish 8-5-1 (Table S4).
arbuscular mycorrhizal fungi. Additionally, fish-treated leek plants
According to information from the OMRI products lists (OMRI,
had twice the shoot weight compared to treatment with conven-
2020a,b), most of these products are produced and sold by compa-
tional fertilizer (Douds et al., 2013). Treatment of lettuce plants
nies based in the US, Canada, and Mexico. However, fish-based
with fish-derived protein hydrolysates significantly increased the
commercial fertilizer products are also on the market in Bermuda,
number of leaves, stem diameter, shoot, and root dry weight of let-
China, Chile, Malaysia, and India. The fish fertilizer products listed
tuce plants (Xu and Mou, 2017). Hydrolysed fish fertilizer was
by OMRI are classified as crop fertilizers and soil amendments
applied in several studies that were conducted by Cox and co-
(OMRI, 2020b). The list, which was updated on January 25, 2020,
workers on calibrachoa and marigold plants (Table 6). This treat-
included a total of 154 products. The products that are allowed
ment gave relatively low shoot dry weight in calibrachoa plants,
by OMRI in accordance with US-NOP standards, included 137 prod-
compared to the mineral fertilizer Plantex (high nitrate 20-2-20)
ucts. These products, assigned to different categories by OMRI,
(Cox, 2010). Calibrachoa plants fertilized with fish fertilizer were
include: (1) Fish Products = 9; (2) Fish Products, Liquid, Stabi-
healthy but smaller than those given Plantex. Nevertheless, based
lized = 74; (3) Fish Products: Multi-ingredient = 19; (4) Fertilizers,
on the plant appearance, the Marigold plants, given either fish or
Blended = 2; (5) Fertilizers and Soil Amendments, Blended = 12; (6)
mineral fertilizer, showed high quality (Cox and Eaton, 2011;
Fertilizers and Soil Amendments, Blended with sodium nitrate, = 2;
Eaton et al., 2013). Application of fish extracts to Chrysanthemum
(7) Fish meal and Powder = 14; (8) Bone meal = 4; and (9) Compost,
plant promoted leaf growth as compared with no fertilizer treat-
other (plant and animal materials) = 1 (OMRI, 2020a,b). However,
ment (Ji et al., 2017).
the OMRI list following COR standards included only 17 products
Foliar concentrations of N in western red cedar (Thuja plicata)
of three categories: (1) Fertilizers, Blended = 4; (2) Fish meal, fish
trees were maximum in trees treated with inorganic fertilizer or
powder, fish wastes, hydrolysate, emulsions and solubles = 12;
fish silage (in combinations with ash). However, the fish silage
and (3) Compost = 1.
treatments resulted in smaller growth response (McDonald et al.,
With few exceptions, most products in the category, Fertilizers
1994).
and Soil Amendments, Blended, most products have either no K or
Fish emulsion-based liquid fertilizer did not show any positive
contain very little K, commonly 1% (Tables S3 and S4). This is a very
effect on soil-borne disease incidence and fruit yield, number,
low figure when compared to the nutritional needs of agricultural
and size in organic greenhouse tomato production systems
and horticultural plants. Complete fertilizers usually contain about
(Giotis et al., 2009). In another study, sandy soil amended with fish
the same amount of N and K, and less P. As referred in Tables S1
emulsion enhanced the growth and development of radish, when
and S2, many fish-based fertilizers contain more P than N. Hence,
combined with bacterial or actinomycete mixture treatments (El-
these fertilizers must be used for top dressing to N-demanding
Tarabily et al., 2003). In studies conducted by Abassi and co-
plants, or for P-deficient soil.
workers, fish emulsion was applied to tomatoes, radish, cucumber,
According to information given for some of the products on
peppers, and eggplant (Abbasi, 2011, 2013) (Table 6). Its applica-
company websites, these products are presented as having the
tion enhanced health and fruit yield of tomatoes and peppers
potential for soil improvement by improving soil microbial activity
(Abbasi et al., 2003), and the growth of radish seedlings (Abbasi
and soil structure and stimulating root growth (Tables S3 and S4).
et al., 2004).
Some of these products can be applied to vegetables, flowers,
OMRI-approved fertilizer products, such as fish emulsion or
shrubs, lawns, tubers, trees, and crop plants. These fertilizers can
feather meal, as sources of N, have been applied usually by US
be applied directly to the soil as a root drench or through foliar
Organic* blueberry farmers. The fish emulsion was given either as
sprays.
a direct liquid application to the soil or through the drip irrigation
system (Julian et al., 2012; Larco et al., 2013a, 2013b). Highbush
6. Scientific studies related to commercially available fish-based blueberry plants fertilized with fish emulsion had more leaf and
fertilizers 1-year-old wood dry weight than those fertilized with feather meal
(Larco et al., 2013a). The Agrothrive and TRUE402 fertilizers
There are 154 commercial fish-fertilizer products that are (Table 6) showed no differences for plant growth, yield, or fruit
allowed by OMRI (Tables S3 and S4), of which very few have been quality, and were considered appropriate for planting establishment
 I. Ahuja et al. / Waste Management 115 (2020) 95–112 105

Table 6
An overview of the scientific studies conducted with commercially available fish-based fertilizer products on different crop plants.

Fish-based fertilizer N-P-K Company name Plant(S) Countries Reference

(Scientific name) on
publication

Agro fish pellet 5-5-2.5* not mentioned Tomato UAE (Kalbani et al., 2016)
(Lycopersicon
esculentum Mill)
Fish meal 10.1-4.5- MadelipOche, Inc., Tomato Canada (Gagnon and Berrouard, 1994)
(Ocean perch) 0.5* Canada
Fish-scale meal W. E. Acres Crabmeal
10.0-3.7- Ltd., Canada
0.1*
6-10-1 6-4.4-0.8* National Sea Products Cabbage Canada (Blatt and McRae, 1998)
Fish bone meal Ltd. of Lunenburg, NS, (Brassica oleracea L.)
(made from ground bones of fresh fish waste) Canada Carrot
(Daucus carota)
Green beans (Phaseolus
vulgaris)
HFPC hydrolysed fish powder 11-0.25-1y Peaceful Valley Farm & Leek USA (Douds et al., 2013)
Garden Supply, Grass (Allium
Valley, CA, USA porrum)
Hydrolysed fish fertilizer 2-4-1 2-1.8-0.8y Neptune’s Harvest Calibrachoa USA (Cox, 2010; Cox and Eaton,
(OMRI certified) Gloucester, MA, USA (Calibrachoa  hybrida) 2011; Eaton et al., 2013)
Marigold
(Tagetes erecta)
Hydrolysed fish fertilizer (Schafer’s Liquid Fish) Not Schafer Fisheries, Yellow squash USA (Ogles et al., 2015)
available Inc., Thomson, IL, USA (Cucurbita pepo)
Collards (Brassica
oleracea var. acephala)
Fish protein hydrolysate Not Conolly Seafood Corn (Zea mays) USA (Randhir and Shetty, 2005)
(a by-product of mackerel processing) available Gloucester, MA, USA
Fish Agra 4-0.4-0.8y Northeast Organics, Blackberry USA (Fernandez-Salvador et al.,
Manchester-by the-Sea, (Rubus subgenus 2015a)
MA, USA Rubus, Watson)
TRUE402 4-0-1.7y True Organic Products,
(fish hydrolysate and fish emulsion with added Inc., Spreckels, CA, USA
molasses)
AgroThrive 2.5-1.1-1.2y AgroThrive, Inc., Morgan
(corn fertilizer; a natural microbial Hill, CA
digestion of corn steep liquor and ground fish
waste)
TRUE402 (fish hydrolysate and fish emulsion with 4-0-1.7y True Organic Products, Blackberry USA (Fernandez-Salvador et al.,
added molasses) Inc., Spreckels, CA, USA (Rubus subgenus 2015a; Fernandez-Salvador
Rubus, Watson) et al., 2015b

Fish hydrolysate 2-4-1y Neptune’s Harvest Sweet basil USA (Parker, 2015)
Gloucester, MA, USA (Ocimum basilicum)
True Organics 5-1-2 5-0.4-1.7y True Organic Products Blackberry USA (Dixon et al., 2016)
(OMRI certified) Inc., Spreckels, CA, USA

OMRI-certified Pacific Natural 2-3-0.3yy Great Pacific BioProducts Tomato Canada (Zhai et al., 2009)
Ltd. (Delta,
BC, Canada)

Fish-derived protein hydrolysates 2-1.3-0.8y C.R. Brown Enterprises, Lettuce USA (Xu and Mou, 2017)
Andrews, NC, USA (Lactuca sativa)
Fish silage Not IBEC Aquaculture Corp. Red cedar Canada (McDonald et al., 1994)
and wood ash available in Port Hardy, B.C., (Thuja plicata)
(3:1 silage-ash by wt.) Canada (9-year old plantation
Western Pulp Ltd. Mill in trees)
Port Alice, B.C.
Fish emulsion samples (made from the whole N 4-6* Omega Protein, Houston, Tomatoes, radish, Canada (Abbasi, 2013; Abbasi et al.,
menhaden fish menhaden fish) (Brevoortia P 1.5-2* Texas/Rockton, Illinois, cucumber (Cucumis 2004; Abbasi et al., 2006;
tyrannus) in commercial operations K 1.2-2.7* USA sativus) Abbasi et al., 2003)
pepper, potato, and
eggplant (Solanum
melongena)
Hydrolyse fish and seaweed fertilizer 2-3-1y Neptune’s Harvest, Bell pepper USA (Russo, 2006)
(OMRI certified) Ocean Crest Seafoods, (Capsicum annum)
Gloucester, Maine, USA

(continued on next page)

106 I. Ahuja et al. / Waste Management 115 (2020) 95–112

Table 6 (continued)

Fish-based fertilizer N-P-K Company name Plant(S) Countries Reference

(Scientific name) on
publication

Fish emulsion-based liquid fertilizer 55-22-55y Nugro, Hortifeeds, Tomato Greece (Giotis et al., 2009)
(g per pot) Lincoln, UK UK
(nutrient
supplied by
Nugro)
Liquid fertilizer Phytamin 801 6-0.6-0.9* California Organic Fescue (Festuca USA (Hartz et al., 2010)
(contained fishery wastes and seabird guano) Fertilizers, Hanford, CA, arundinacea) turf
USA
Fish emulsion 5-0.9-1.7y Agro-K Corporation, Basil (Ocimum USA (Treadwell et al., 2011)
Minneapolis, MN, USA basilicum)
Spearmint (Mentha
spicata)
Fish emulsion 4-0.4-0.8y Northeast Organics Inc., Blueberry USA (Julian et al., 2012; Larco
(Fish Agra) Manchester-by-the-Sea, (Vaccinium et al., 2013a; Larco et al.,
y
3.6-0.6-5.2 MA, USA corymbosum) 2013b)
Yates fish emulsion 4.5-1.8-1.2y Arthur Yates & Co Radish UAE (El-Tarabily et al., 2003)
(made from pure fish residue) Limited, Milperra, (Raphanus sativus) Australia
NSW, Australia) Egypt
Fish waste (liquid) Not JK Organic fertilizer Tomato Brazil (Roldi et al., 2013)
(a commercial preparation) available
Fish extracts 91.3-13.6- Yirong Bio-engineering Chrysanthemum China (Ji et al., 2017)
(China OFDC certified organic) 48.5 Co. Ltd., Ningde, Fujian, (Chrysanthemum
(g/L)* China morifolium)
*
N-P-K contents as per analyses done by the authors themselves or in collaboration with other laboratories, as mentioned in respective studies.
y
N-P-K contents as provided by the fish product selling companies as per the information gathered from studies.

in blackberry (Fernandez-Salvador et al., 2015a). Blackberry culti-
vars, after fertilization with TRUE402, Phyta-GrowÒ Leafy Green
SpecialTM (pelletized soy meal), and pelletized processed poultry
litter showed a similar response to these fertilizers (Fernandez-
Salvador et al., 2015b).
These studies show that a number of commercial fish-based fer-
tilizers have increased the growth of several horticultural and
ornamental plants, as well as maize (corn) and young trees. For
crops such as cereals, ley, and potatoes, studies with these com-
mercial fertilizers are scarce. This may reflect that these commer-
cial products may be costly to apply in arable crops and leys, or
that they may be more suitable for horticultural or ornamental
plants. Besides, for many organic* vegetable growers, management
of N is crucial, especially those producing high N-demanding crops
(Hartz and Johnstone, 2006; Ogles et al., 2015). The application of
hydrolysed fish fertilizer as an in-season supplement can be the
source of quickly available N. Thus, hydrolysed fish fertilizer is sug-
gested as a prospective economic option in organic* farming (Ogles
et al., 2015).
7. Effect of FW-based non-commercial fertilizers on plants
As per literature search, a limited number of studies have been
carried out that used FWs to develop non-commercial fish-based
fertilizers and also reported the effects of FWs on plants.
7.1. Effect of FW-based liquid fertilizers on plants
Fish-based liquid fertilizers have been produced from FW using
starter cultures, and through the process of fermentation. Such fer-
tilizers, produced by scientists, have been tested on a range of
plants. Researchers from the USA applied fish soluble nutrients
over seven years in greenhouse and field trials covering a broad
range of crop plants, such as lettuce, radish, sorghum, sweet corn,
peas, and soybean (Aung and Flick, 1980; Aung et al., 1984). Fish
soluble nutrients were observed to be beneficial, provided that
the fertilization was done with moderate dilution. In a study from
India, liquid fertilizer was prepared from FW, amended with Bacil-
lus subtilis bacterial culture and sterile water (Aranganathan and
Rajasree, 2016). Tomato plants treated with this fertilizer showed
good growth response as compared to fertilization with diammo-
nium phosphate. Liquid fermented fish used with the trade name
Gunapaselam” was prepared and tested on soil and different
plants (Balraj et al., 2014; Hepsibha and Geetha, 2017; Vincent
et al., 2014). Its application decreased the soil pH and enhanced
the exchangeable cation levels, organic carbon, organic matter,
and N, P and K of brinjal (Solanum melongena Linn.) plants. Guna-
paselam was indicated to be a valuable resource for enhancing soil
fertility and plant growth (Balraj et al., 2014). Its application as soil
amendment enhanced plant growth and root length of green gram
(Vigna radiata) plants (Hepsibha and Geetha, 2017).
In different studies from Ethiopia and South Africa, following
the methodology given by Abera et al. (2008), FW of Nile Tilapia
was used to prepare liquid fertilizer (Ihemanma and Ebutex,
2013; Lema and Degebassa, 2013). The fertilizer boosted the pro-
duction of tomato (Lycopersicon esculentum) plants at a later age
and was considered to be used as an alternative to the fertilizer
diammonium phosphate for tomato (Ihemanma and Ebutex,
2013; Lema and Degebassa, 2013). In a study from Malaysia, liquid
fish silage was prepared from FW (non-edible parts) of tread fin
seabream (Nemipterus japonicus) by mixing emulsified FW with
molasses and Lactobacillus acidophilus (Fagbenro and Jauncey,
1995; Karim et al., 2015). Fish silage at concentrations of 5.0, 7.5,
and 10% produced comparable plant growth, yield, pigment con-
tent, and post-harvest quality in pakchoi (Brassica rapa L. subsp.
chinensis), compared to plants that were given commercial fertil-
izer (N-P-K; 15:15:15) (Karim et al., 2015).
7.2. Effect of FW-based compost on plants
Application of compost produced from by-products of Sar-
dinella (Sardinella orita) as soil amendments to millet (Pennisetum
glaucum) and groundnut (Arachis hypogaea) showed that FW has
the potential to increase crop yields. However, its effect on yields
 I. Ahuja et al. / Waste Management 115 (2020) 95–112
varied across farms showing the non-uniformity of the by-
products and methods of processing across villages (Ndiaye et al.,
2000).
The potential of the FW-based compost was assessed to design
new fertilization programs in organic* agriculture (Illera-Vives
et al., 2015b; Illera-Vives et al., 2017). Compost from FW mixed
with seaweed was found to be a suitable soil amendment for hor-
ticultural crops as observed with yields obtained from tomato and
lettuce plants. Application of compost at a rate of 66 t ha
1 fresh
wt. (FW) (total N: 765, total P: 236, and total K: 317 kg ha
1), sig-
nificantly increased tomato yields. This was associated with
increased fruit weight and larger fruit diameter compared to crops
receiving mineral fertilizer or no fertilization (Illera-Vives et al.,
2015b). The compost residual effect was significant, which led to
higher commercial yields for lettuce in comparison to control
and mineral fertilizer applications. The similar kind of compost in
another study by the same researchers, when applied at a rate of
65 t ha
1, enhanced potato production by 30% relative to mineral
fertilizer, and by 53% to the use of no fertilizer. The compost was
suggested as a beneficial fertilizer for potato cropping in organic*
agriculture (Illera-Vives et al., 2017).
The highest crop yield of maize (Zea mays L.) was observed in
composts containing mixtures of FW with straw and lignite (brown
coal), and FW with bark and lignite (Radziemska and Mazur, 2015).
Soil fertilization with compost from FW and pine bark increased
fresh and dry matter yield of leaves of ice lettuce (Lactuca sativa
L.)., and the concentrations of macro and secondary nutrients.
Additionally, the treatment improved the K:(Mg + Ca), K:Mg, and
K:Ca ratios; however, the Ca:P ratio decreased (Radziemska et al.,
2018). The FW from tilápia beneficiation2 (Enviro-Fish Africa.,
2006), after composting with crushed grass, was examined as a
source of humic acids to promote the growth of lettuce plants
(Busato et al., 2018). A concentration of humic acid extract (20 mg
L
1) significantly enhanced dry and wet root matter in lettuce.
As discussed, a broad range of products have been studied,
many of which showed positive effects on a variety of crop plants.
Fish-based fertilizers can be produced in very different formula-
tions, solid and liquid. Altogether, it seems that they are most often
applied to provide N, or in a combination of N and P, and some
cases to enrich a compost; and less often as a complete fertilizer
to cover all the nutritional needs of a crop.
8. The fishing industry and FW-utilization in Norway
8.1. Norwegian fishing industry
The Norwegian fishing industry includes value chains based on
the harvesting of cod varieties, pelagic species, flatfish, and benthic
species, shellfish, and other molluscs. These value chains include
collection, processing, and sales/export activities (Eurofish
International Organisation, 2019; Olafsen et al., 2012). In the past
30–40 years, the fishing industry has changed significantly, from
a situation with almost free access to fishing – towards highly reg-
ulated fishing, with fewer fishers and vessels (Regjeringen.no,
2017). The regulation of Norwegian fisheries is based on interna-
tional law and cooperation (Eurofish International Organisation,
2019; Ministry of Fisheries and Coastal Affairs, 2007). In 2017
and 2018, Norway was the 9th largest capture fishery nation in
the world (FAO, 2019, 2020). The marine capture landings (live
weight equivalents) from 2002 to 2019, were in the range of 2.2
to 2.8 million tonnes (Directorate of Fisheries, 2020). The amount
of captured fish exported by Norway has varied over the years,
from about 1.79 million tonnes in 2009, 1.86 million tonnes in
2
Beneficiation processes refer to activities that add value to raw materials.
107
2010, and ranging between 1.41 and 1.63 million tonnes in other
years (Fig. S1A). However, the export value of captured fish has
increased steadily from 2014 to 2019, from about (22.50–30.80 bil-
lion NOK) (Fig. S1B) (Seafood.no, 2020).
8.2. Utilization of FW to produce marine ingredients
The amounts of captured fish (white and pelagic fish), and shell-
fish brought on board to ships processing the FW into a meal, oil,
etc., or brought to shore for processing, is about 1.8–2.2 million
tonnes per year (Fig. 2A, Base of raw material (BoRM). About 24–
26% of this raw material consists of heads, backbones, intestines,
roe, milk, etc., which are available for further utilization (Fig. 2A,
available RRMs). The FW is either referred to as ‘‘raw materials”
or ‘‘residual raw materials” (RMs/RRMs) in Norway. Most RRMs
coming from pelagic fish are utilized. Also, there has been an
increase in the utilization of RRMs coming from white fish over
time (Fig. 2B). For shellfish, the utilization of RRMs has been less,
but this comprises a minor volume as compared with white fish.
Currently, there are more than 60 Norwegian companies spe-
cialized in using RRMs to produce marine ingredients. The activi-
ties of these companies are categorized as: Silage conservation
and refining, Fish meal factories, Enzymatic hydrolysis (fish protein
hydrolysates, Products for human consumption, and Frozen fish back-
bones & cuts for fur farmers, and Fish processing companies within the
white fish industry (Richardsen et al., 2019).
The quality requirements about RMs are given under the ‘‘Reg-
ulations about quality on fish and fish Products” (Lovdata, 2013).
Some of these requirements for different kinds of RMs are briefed
in Table S5. For instance, these include requirements regarding the
use of RMs in the production of fishmeal, fish protein hydrolysate,
and other marine ingredients for human consumption, and for RMs
that can be used for other purposes.
8.3. Potential for utilization of FW as fertilizers
There has been an increase in the utilization of FW from white
fish from less than 40% in 2012 to almost 60% in 2018 (Fig. 2B).
These 60% of utilized material amount to about 300.000 tonnes,
and the remaining 40% (~120.000 tonnes) per year is still available,
which is a significant amount of material. Assuming that, the FW
contains 30% DM, and 10% of DM is P (Table 2), this amounts to
3900 tonnes of P annually. In 2018, in Norway, the annual applica-
tion of P as animal and mineral fertilizers was 15.600 tonnes (SSB
Statistics Norway, 2020). Hence, utilizing FW for fertilization in
agriculture could significantly reduce the current dependency on
importing P in phosphate rock. P is also on the list of the EU’s cru-
cial resources (European Commission, 2017a). FWs (fish bones) can
be utilized to produce P, for example, through solubilization of fish
bones (Wyciszkiewicz et al., 2017), or by directly using hydrolysed
fish bones for fertilization (Ahuja and Løes, 2019).
Until now, a significant amount of FW from white fish has been
applied as feed for fur animals. This use is currently hampered due
to a ban on keeping fur animals in Norway (Lovdata, 2019). Farm-
ers who have had fur animals before January 2018 can keep them
until February 2025; after this date, fur farming will be banned in
Norway. Due to this changing situation, there is a window of
opportunity for establishing an industry for marine-derived fertil-
izers. Currently, some open sea fisheries with on-board processing,
dump RRMs in the sea due to limited storage on ships. However,
new ships are being equipped with storage solutions for all the
catch volumes, increasing availability of RRMs for fertilization pur-
poses. These developments create additional opportunity for
establishing a marine-derived fertilizer industry.
108 I. Ahuja et al. / Waste Management 115 (2020) 95–112

Fig. 2. Raw materials (RMs) from different sectors of wild fish capture, availability and utilization of residual raw materials (RRMs) that came from sectors of wild fish
capture, during 2012–2018 (Richardsen et al., 2019). A. Base of raw material (BoRM) and available residual raw materials (aRRMs) from sectors of the capture of white fish,
pelagic fish, shell fish. B. Utilization (%) of residual raw materials from sectors of capture of white fish, pelagic fish, and shell fish.

9. Conclusions phosphate rock. FW can be processed in many ways to produce

Taken together, we have brought forward how FW, especially
solid FW, can be processed to produce fertilizers for organic* farm-
ing, advancing sustainable management of FW and organic* agricul-
ture. Different studies both on commercial and non-commercial
fish/FW based fertilizers and in different countries demonstrate a
positive impact on plant growth. However, fish/FW based fertilizers
have been tested mostly on horticultural plants. The OMRI institute
provides a comprehensive overview of fish-based fertilizers that are
allowed for use in certified organic* farming. Information available
about these products also indicate the potential for soil improve-
ment by improving soil microbial activity and soil structure and
stimulating root growth. However, more information is required
about the applicability of commercial fish-based fertilizers to vari-
ous crops, especially agricultural crops.
Utilization of residual raw materials, for instance, as FW based
fertilizers fit well with the EU’s circular economy policy. These
recycle scarce minerals from the sea and back to terrestrial envi-
ronments. FW based fertilizers are most often applied to supply
N or a combination of N and P to crops. In organic* farming, hydrol-
ysed fish fertilizer can be a good source of N for N-demanding
crops. Besides, these fertilizers can address issues of limited access
to mineral P fertilizer and reduce dependency on importing P in
both liquid and solid fertilizers and can be combined with other
ingredients, for instance, to produce fish-based composts, diges-
tates or FW-seaweed fertilizers.
With increasing focus on organic* growing in Europe and in Nor-
way, the increased availability of FW in Norway provides an inter-
esting source of raw material that may replace currently applied
fertilizers such as dried poultry manure form conventional farming.
OMRI-listed products are mostly produced and sold from compa-
nies based in the US, Canada, and Mexico; thus, indicating a poten-
tial to produce marine-derived fertilizers in European countries.
Declaration of Competing Interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
Acknowledgements
This publication has been funded by The County Council of Møre
and Romsdal through the project entitled ‘‘Marine rest raw mate-
rials for fertilizers to organic agriculture” (RESTOR).
 I. Ahuja et al. / Waste Management 115 (2020) 95–112 109

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