1. A review of feed in finfish
aquaculture
Current and future prospects
Christopher Michael White
Student #: 10406689
August 31st 2013
University of Amsterdam
Faculty of Science: Master Biological Sciences
Track: Limnology and Oceanography
Supervisor: Dr. Ir. J.M. de Goeij
Examiner: Dr. H.G. van der Geest
5. Abstract
Industrial finfish aquaculture has historically been widely considered an inefficient
way to grow fish that is neither sustainable nor ecologically friendly. Direct neg-
ative effects of finfish aquaculture can include habitat destruction, waste disposal,
exotic specie introductions, spreading of pathogens, and depletion of food stocks
for predator fish in the form of harvesting small pelagic fish for feed production.
These factors present significant hurdles to overcome, yet feed presents the greatest
opportunity for the industry to become more effecient. Here, I discuss the various
feeds in use today including wild catch, bycatch, terrestrial animal rendered feed,
terrestrial crops, periphyton, as well as future prospects including single celled or-
ganisms and insects. By providing an overview of feed limitations, efficiency, and
prospective uses, I hope to provide the reader with an overview of the current indus-
try, the driving influences of a market driven economy, and the potential directions
the industry will take in regards to feed.
1
6. Contents
Definitions
Aquaculture - The production of all farm raised aquatic based organisms used for
food consumption or secondary value products such as feeds, medicines, and oils.
Aquafeed - Any feed product, marine based or terrestrial based that is fed to rear
fish and other aquatic organisms within aquaculture. It may or may not include
fishmeal or fish oil.
Docosahexaenoic acid - A highly unsaturated fatty acid comprised of a 22 carbon
chain.
Eicosapentaenoic acid - A highly unsaturated fatty acid comprised of a 20 carbon
chain.
Extensive farming systems - No outside feed or nutrient input is used during the
process of rearing fish within fish farms.
Fish feed - Any feed product, marine based or terrestrial based that is fed to rear
fish within aquaculture. It may or may not include fishmeal or fish oil.
Fishmeal - Fish feed that is 100% in origin from wild catch fisheries and or bycatch.
Fish in : Fish out - The ratio between weight of wet fish entering processing for
fishmeal production and the weight of the farmed fish reared off the fishmeal.
Fish oil - Fish oil that is 100% in origin from wild catch fisheries.
Highly unsaturated fatty acid - comprised of 20 or more carbon atoms with more
than 4 unsaturated bonds.
Intensive farming systems - A complete and external diet meeting all nutritional
needs is provided during the process of rearing fish within fish farms.
Linoleic acid - A unsaturated fatty acid comprised of a 18 carbon chain; a precursor
to Docosahexaenoic and Eicosapentaenoic acid.
Manufactured aquafeed - Industrially produced, often sourced from multiple raw
foods, fillers, minerals, and vitamins.
Polyculture - Ecological diversification of aquaculture through the rearing of at least
two species within a farm that exhibit distinct ecological niches.
Polyunsaturated fatty acid - comprised of a less than 20 carbon atoms with multiple
unsaturated bonds.
Semi-intensive farming systems - A supplementary diet containing either fertilizers
or external fish feed, provided during the process of rearing fish within fish farms.
Wet fish mass - The weight of fish when it is still whole before it enters into pro-
cessing.
2
7. Contents
Abbreviations
DHA - Docosahexaenoic acid
EFS - Extensive farming systems
EU - European Union
EPA - Eicosapentaenoic acid
FAO - Food and Agricultural Organization
FCR - Feed conversion ratios
FI:FO - Fish in : fish out
HUFA - Highly unsaturated fatty acid
IFFO - International Fishmeal and Fish Oil Organization
IFS - Intensive farming systems
LA - linoleic acid
MA - Manufactured aquafeed
MBM - Meat and bone meal
PBM - Poultry byproduct meal
PUFA - Polyunsaturated fatty acid
SCO - Single celled organisms
SIFS - Semi-intensive farming systems
3
8.
9. 1 Introduction to fish aquaculture
and aquafeed
1.1 Growth in aquaculture and the finfish industry
The aquaculture industry is growing at a rapid pace, becoming a significant contrib-
utor to global seafood supply. In 2010, capture fisheries and aquaculture generated
148 million tons of aquatic based organisms, valued at 217.5 billion US dollars ac-
cording to the Food and Agricultural Organization of the United Nations (FAO),
fisheries and aquaculture department [1]. The contribution of aquaculture to overall
aquatic based food consumption has dramatically increased in recent decades, ex-
periencing a 3.2% growth rate since 1961 and a 5% growth rate over the last decade
[1, 45]. This has led to the aquaculture industry expanding by more than a factor
of ten over the past three decades, now producing an annual 63.6 million tons of
aquatic organisms (excluding aquatic plants and non-edibles), representing roughly
40% in volume to that taken in by capture fisheries (Fig. 1.1) [1].
Figure 1.1: FAO depiction of global catch of all aquatic organisms and aquaculture
production [1]
More specifically, finfish aquaculture represents a significant portion of overall aqua-
culture. The production of farmed finfish in 2010 was 39.2 million tons which is
more than half of all aquaculture production, again excluding aquatic plants and
non-edibles [1]. Since finfish aquaculture is rapidly becoming a significant portion of
5
10. Chapter 1 Introduction to fish aquaculture and aquafeed
global aquatic food supply, the feed that is required to sustain the industry will con-
tinue to see an increase in demand. Therefore, it is important to focus on feed and
investigate the origins, pitfalls, governance, and whether it is sustainably sourced
to see if the finfish aquaculture industry is able to continually grow. However, the
farmed finfish industry can be divided into three farming types based on different
feed requirements and this needs to be taken into consideration when discussing the
industries prospects in regards to feed.
1.2 Overview of finfish farming systems
There are three broadly classified feeding categories that finfish aquaculture falls
under. The first is an extensive farming system (EFS), in which no additional
feed is provided to herbivorous, omnivorous, and detritivorous fish. The second
fishery type is semi-intensive farming system (SIFS). SIFSs like EFSs, are often
found on a local scale, such that they are often run by individuals or households,
but differ as SIFSs typically use whatever is locally available as an additional feed
source. Direct inputs can range from local household food waste to manufactured
aquafeed. Other feed sources used such as manure, actually add nutrients to increase
primary productivity, thereby indirectly increasing the food source for the farmed
species [51, 17]. Lastly, intensive farming systems (IFS), are represented in large
part by consumer desired carnivorous fish such as salmon and trout in which all
feed requirements are provided from an external source.
Of the finfish sector, the majority of production is generated by EFSs and SIFSs that
raise fresh water carp within Asia. The top 10 producing countries for aquaculture
represent over 80% of the market share both in volume and value, while China
alone represents 60% of global aquaculture production [1]. The production of fresh
water farmed finfish stands at 33.9 million tons, or 86.5% of the finfish aquaculture
industry [1]. Marine farmed fish contribute to a much lesser extent at 3.4 million
tons, followed by brackish farmed fish at 1.9 million tons in 2010 [1]. 24.2 million
tons of fresh water carp were harvested in 2010, making it the largest contributor
to the industry, representing 62% of all farmed finfish (Fig. 1.2) [1, 45].
6
11. 1.2 Overview of finfish farming systems
Figure 1.2: FAO depiction of types of farmed finfish and relative amounts produced
globally; note the variable x-axis per figure. [1]
7
12. Chapter 1 Introduction to fish aquaculture and aquafeed
One can see that the industry is weighted heavily towards the production of fresh
water herbivorous species. This could be considered a positive aspect of the fin-
fish aquaculture industry as these fish require less feed than carnivorous fish such
as salmon and trout. However, this trend is changing as farmers try to increase
yields. Despite the fact that 50% of all carp production was non-fed in 1980, the
number has fallen to 33.3% in 2010, as farmers attempt to increase yields by the
implementation of additional feeding practices [1]. While SIFSs are thought to yield
approximately 0.5 − 20t/ha/yr of fish, IFSs which are completely dependent on
manufactured aquafeed (MA), are able to operate at a much larger scale, resulting
in farms producing 1000t/ha/yr of fish [51, 17]. Despite the fact IFSs often require
extensive setup and costly feed input, it is easy to see how operators of EFSs and
SIFSs are moving towards using more complicated feed sources with the prospects
of increase yields. As it stands, most fish feed is destined for IFSs and to a lesser
extent SIFSs, although there is a shifting trend towards intensification and the use
of manufactured aquafeed within SIFS [51, 17]. As this intensification occurs, it is
important to investigate if fishmeal and fish oil production can keep up with this
growing demand from the farmed finfish industry.
1.3 Current use of fishmeal and fish oil within
aquaculture
In recent years, the increasing size of the finfish aquaculture industry has resulted
in fishmeal and fish oil to become more scarce and more expensive as pelagic wild
caught fish processed into fishmeal and fish oil become fully exploited and in some
cases over exploited. The FAO defined the state of world fisheries in 2012 as follows,
“The declining global catch over the last few years together with the increased
percentage of over exploited fish stocks and the decreased proportion of non-fully
exploited species around the world convey a strong message; the state of world
marine fisheries is worsening and has had a negative impact on fishery production
[1].”
The FAO estimated as of 2009, that the majority of the 10 top fisheries repre-
senting 30% of capture fish stocks were either fully exploited or over exploited
[1]. They listed the following fisheries as fully exploited; the two main stocks of
anchoveta* (Engraulis ringens) in the Southeast Pacific, Alaska pollock (Thera-
gra chalcogramma), Atlantic blue whiting (Micromesistius poutassou), Atlantic her-
ring* (Clupea harengus), and the Chub mackerel* (Scomber japonicus) stocks in
the Eastern Pacific and the Northwest Pacific [1]. Additionally, the FAO has listed
the Japanese anchovy* (Engraulis japonicus) and the largehead hairtail (Trichiu-
rus lepturus) in the Northwest Pacific, as well as Chilean jack mackerel* (Trachurus
murphyi) in the Southeast Pacific as over exploited [1]. Many of these stocks happen
8
13. 1.3 Current use of fishmeal and fish oil within aquaculture
to be pelagic foraging fish, and those designated with an (*) represent the very same
fish targeted for capture and processing into fishmeal and fish oil [40]. The world
catch and aquaculture usage can be seen in Fig. 1.3. The amount of sea food (ex-
cluding aquatic plants) not directly consumed by people and destined for non-food
purpose in 2010 was over 20 million tons, 15 of which went towards the production
of fishmeal and fish oil [1].
Figure 1.3: FAO depiction of world fisheries utilization in 2010 [1]
These exploitations of small pelagic fish has recently led to reductions in their avail-
able catch and thus limited the production of fishmeal and fish oil. This can be
observed by the correlation between catch, production of fishmeal and fish oil, and
the rising cost of these commodities. Wild anchoveta caught off the coast of Chile
and Peru reflects the strongest correlation as this fishery accounts for 40% of the
total production of fishmeal and fish oil [41]. 12.5 million tons of anchoveta were
caught in 1994 and since then, there has been a drastic reduction in yearly catch to
4.2 million tons in 2010 [1]. These reductions have largely been attributed to closures
on fisheries by the Peruvian government. During the same time frame, historical
fishmeal production peaked in 1994 at 30.2 million tons (live weight equivalent),
followed by reductions to 15.0 million tons in 2010 [1]. Due to the limitations of
harvesting the Peruvian anchoveta, the cost of fishmeal and fish oil have both risen
dramatically over recent decades. For fishmeal bought in the Netherlands and Ger-
many, the cost has risen from $300 per ton in 1985 to $1,300 per ton at the beginning
of 2012, while similar price hikes of $300 per ton, increased to $1,600 per ton for fish
oil [1]. This is a serious concern for fish farmers as it is estimated that feed makes
up 75% of all costs [45].
9
14. Chapter 1 Introduction to fish aquaculture and aquafeed
1.4 How can the industry grow with limited fishmeal
and fish oil?
If the world is to maintain current levels of per capita fish consumption, we will
have to produce an additional 23 million tons of aquatic animal food by 2030 [1].
With the limited ability for the wild catch sector to increase as most wild stocks
are fully exploited and in the the case of the Peruvian anchoveta, either decreasing
or stabilizing to a constant level, it is clear other sources of feed will play a pivotal
role in the future of aquafeed to maintain growth. Contrary to mainstream beliefs,
the incorporation of other feed sources with fishmeal and fish oil is already well
under way and widespread throughout the farmed finfish aquaculture industry. A
review of the 2006 global aquaculture statistics by Tacon and Metian 2008, showed
that of the 25.36 million tons of aquafeed used, 20.81 million tons or 82% originated
from non fishmeal or fish oil sources [53]. These sources include terrestrial animal
rendered meal from animal farming byproducts and comes in the form of meat and
bone meal (MBM), blood meal, poultry byproduct meal (PBM), and feather meal.
In addition, there are various crop based meals originating from soy beans, wheat,
and corn amongst others. Oils in use to supplement fish oil originate from sunflower,
linseed, canola, rapeseed, olive, and palm to name a few [41]. These new sources of
feed are already having an impact as the inclusion level by percentage of fishmeal
and fish oil within aquafeed are on the decline for all farm raised fish (Tab. 1.1).
Table 1.1: FAO predictions for reduction of fishmeal inclusion within aquafeed over
time. [52, 1]
The limitations of fishmeal and fish oil as well as their drastic increases in prices,
coupled with the growing global aquaculture industry has caused the drastic shift
10
15. 1.4 How can the industry grow with limited fishmeal and fish oil?
towards new fish feed types, mixes, and solutions to this pressing problem. This
raises a few questions. How do these new feed sources compare to traditional fish-
meal and fish oil? What are the ecological risks and benefits and most importantly,
will the industry be able to sustainably source these new feed types? The answers
to these questions are vital if the finfish aquaculture industry is to maintain its pro-
jected growth. It is my intention to outline the major aquafeed sources currently in
use followed by potential feeds not yet used. In regards to each feed type, I intend
to summarize their scale, benefits and pitfalls, governance, and future prospects
within the finfish aquaculture industry. My hope is that this provides insight into
the potential directions of feed use within finfish aquaculture, thereby giving differ-
ent stakeholders the opportunity to steer the industry towards more efficient and
sustainable practices. When considering the use of alternative feeds, it is first im-
portant to understand the process of energy conversion from wild fish into fishmeal
and fish oil so that the merits of this feed type can be properly compared to other
aquafeed discussed later on.
11
16.
17. 2 The real cost of fishmeal and fish
oil
There are a number of tools used by the scientific community for measuring energy
conversion and efficiency of finfish aquaculture. These tools, chiefly feed conversion
rates (FCRs) and fish in: fish out (FI:FO) ratios, are becoming less applicable
as alternative aquafeeds are incorporated with fishmeal and fish oil. Additionally,
when the conversions are broken down, one can see that the use of pelagic fish as
feeds are still highly inefficient. Other energy requirements that are not taken into
consideration include fuels required to run fishing vessels out to catch the pelagic fish,
operation of the fishmeal factories, and the transport needed to move the fish feed
to the fish farm. Considering that developing countries make up 35% of fishmeal
and fish oil exports by quantity, and Europe conversely imports 45.9% of these
commodities, the amount of energy used in these processes should not be ignored
when compared to other feed types [1, 54].
2.1 Feed conversion ratios
3.7 million tons of fishmeal were used by the aquaculture industry in 2006, represent-
ing 68.2% of the fishmeal market while 835,000 tons of fish oil was used, representing
88.5% of the fish oil market [53]. A feed conversion ratio (FCR) describes the con-
version of feed to fish, but it neglects the other side of the equation in which pelagic
forage fish are turned into feed. Studies mapping the industry in 2006, showed that
1 kg of “wet fish” or whole fish yielded 0.225 kg (22.5%) fishmeal and 0.05-0.07 kg
(5-7%) fish oil after processing [49, 4, 53]. More recent data from the International
Fishmeal and Fish Oil Organization (IFFO), has put the conversion ratio of fishmeal
at 24%, citing more efficient protein recovery methods [29]. These conversion rates
largely stem from the anchoveta and Pacific mackerel caught off the west coast of
South America, destined for processing into fishmeal and fish oil [4]. If we continue
working with the Tacon and Metian 2008 statistics and take the total amount of
aquafeed used in 2006 (25.36 million tons), and subtract the fishmeal (3.7 million
tons) and fish oil contributions (0.835 million tons), we can see that the remaining
feed makes up 81% of the total [53]. A visual break down can be seen in Fig. 2.1.
This means that the fishmeal and fish oil used in 2006 translates to 19% of the to-
tal aquafeed [53]. The total yield of farmed fish and crustaceans fed manufactured
13
18. Chapter 2 The real cost of fishmeal and fish oil
aquafeed in 2006 was 15.07 million tons [53] Taking the manufactured aquafeed and
fish yield for 2006, we can calculate an average FCR of 1.68 for fish and crustaceans.
Figure 2.1: Visual representation of 2006 aquaculture input and output. Adapted
from Tacon and Metian 2008, Shepard 2005, and Anon 2006. [53, 49, 4]
It should be noted that in the Tacon and Metian 2008 paper, there is no mention of
what an additional 8.78 million tons farmed fish and crustaceans are fed, although
i assume aquafeed produced on a local scale with local farming practices. It does
however highlight the difficulties of mapping an entire input and output for any given
year and therefore could contribute a source of error. Within the same year, there
was also 9.42 million tons fish raised from EFSs and 4.14 million tons of miscellaneous
marine crustaceans and minor cultivated species. This is important to mention as
significant yields are obtained without manufactured aquafeed shows the diversity
of aquaculture around the world. One will also note I have calculated the pelagic
fish not destined for compound aquafeed but harvested for use as terrestrial animal
feed and fish oil products. This FCR of 1.68, calculated from the 2006 data agrees
with the average FCR for all major species using compound aquafeed in 2006, most
ranging between 1 and 2.5 [53, 18]. However, the flaw of FCRs are evident from
Figure 2.1 as they do not take into account the conversion of 16.6 mt pelagic fish used
to create a fraction of the manufactured aquafeed. Furthermore, it is impossible to
deduce an overall energy conversion of manufactured aquafeed as the input required
to make 20.81 million tons of terrestrial sourced aquafeed is diverse and difficult to
quantify.
14
19. 2.2 Fish in : fish out
This said, the average FCR for the top 10 farmed fish in 2000, which stood at 1.9 has
come down and is estimated to continue to fall in the coming years (Tab. 2.1) [40].
This can be attributed in part to farming systems becoming more efficient with
their feeding methods, continual development of feeds, and improved fish rearing
methodologies. Thus, FCRs may act as a standard to measure feed improvements
but fail to convey overall efficiency of inputs and outputs. What one can take out
of this is that there still exists a significant energy gap between input and output
for fish raised on manufactured aquafeed.
Table 2.1: FCRs of major farmed species set to fall. Adapted from Tacon and
Metian 2008, FAO 2008. [53, 18]
Fish type 2006 2015 2020
Salmon 1-1.6 - 1.3
Trout 0.7-2 - 1.3
Tilapia 1.3-2.6 - 1.5
Chinese carp (non-filter feeders) 1.3-2.5 - 1.5
Catfish 0.9-2.9 - 1.3
Milkfish 2.0 1.7 -
2.2 Fish in : fish out
If one looks at the other big measurement tool used to measure efficiency within
the industry, equally large flaws are observed. Although the methodology for fish in
: fish out (FI:FO) ratios is debated in the literature, Jackson 2009, seems to have
improved the concept by creating a more accurate FI:FO ratio through the use of
the following equation [53, 29].
FIFO Ratio = ((Level of fishmeal in the diet + level of fish oil in the diet) / (yield
of fishmeal from wild fish + yield of fish oil from wild fish)) * FCR
Using salmon as an example, Jackson 2009 calculated the FI:FO as follows. FIFO
ratio = ((30% + 20%) / (22.5% + 5%)) * 1.25 = 2.27:1 [29]
This again provides insight as it allows us to calculate the kgs of pelagic fish required
to produce a kg of salmon, but in an industry that is radically moving away from
using fishmeal and fish oil as an input, it fails to address the impact of the other
feed input. So if we look as this salmon example presented by Jackson 2009, only
50% of the input is considered while leaving out the cost of the other half of non
fish sourced diet, or aquafeed. A FI:FO ratio therefore gives a better idea of the fish
conversion cost, but it too fails as a true measurement standard when considering
fish raised on manufactured aquafeed as it does not take into account the 81% of
non fishmeal and fish oil included in aquafeed for 2006. Additionally, a FCR ratio
is used within the FI:FO equation which was shown previously to fall victim to the
15
20. Chapter 2 The real cost of fishmeal and fish oil
realized feed conversion cost, thereby compounding the error. We therefore need to
be vigilant of the inherent flaws when considering FI:FO ratios and FCRs.
2.3 Direct consumption of pelagic fish
One final consideration in regards to the production of fishmeal and fish oil for
aquafeed is the other uses of pelagic forage fish that may provide a valid argu-
ment for a more valuable end product. The direct consumption of pelagic fish is
more energetically efficient than eating fish raised on fishmeal and fish oil and is
increasingly competing for the pelagic fish market. Methods are being improved to
allow the harvesting and use of small pelagic fish within a variety of food products.
Pelagic forage fish are now incorporated within more than 19 food products includ-
ing powders, fish nuggets, noodles, canned marinates, dried products and protein
concentrates amongst others [54]. Although only 0.73% of the Peruvian anchovy was
destined for human consumption in 2006, it is more than double what was consumed
by people in 2002 [54]. This exemplifies another pressure on the market for small
pelagic fish as demand for direct consumption increases. This in conjunction with
the inefficiencies of fishmeal and fish oil provide the strong case that other aquafeed
sources should be used to feed fish when possible. This however depends on their
own ecological footprint and feasibility to act as aquafeed.
16
21. 3 Alternative aquafeed
considerations
Replacement feeds need to meet certain criteria before they can be used as fish feed
in finfish aquaculture. A feed needs to be palatable and digestible by fish, promote
growth, and the health of the fish. It needs to be readily available and ship easily as
well as handle temporary storage. It has to have consumer acceptance and promote
human health as fish oil and fishmeal do. Finally, it has to contribute minimally
to the environmental footprint when regarding the feed production itself as well
as the resulting effluent [41, 24]. These conditions need to be met if the aquacul-
ture industry is to have any chance of locating long lasting alternative aquafeeds to
replace fishmeal and fish oil. From these challenges in particular are dietary require-
ments of fish that aquafeeds have to meet. The following section briefly discusses
this challenge to provide the reader with a foundation of dietary requirements when
considering alternative aquafeeds.
3.1 Fish Physiology
As manufactured aquafeed increasingly becomes a synthesis of multiple
ingredients, the dietary components become increasingly important to understand.
Fish diets are based on two major components; proteins representing roughly
18-50% of the diet and lipids at roughly 10-25% of diets. Some species like talapia
may require 40-60% protein in their diets while some salmon require over 65%
protein in their diets [47]. This is the reason why fish have been found to be a
fundamental source of dietary protein with an estimated 1.25 billion people using
fish for 25% or more of their daily protein intake world wide [54]. An overview of
the protein content that various types of feed provide, can be seen in Tab. 3.1.
More specifically, of the 20 amino acids that represent the building blocks for
protein, most fish species are unable to synthesize 10 of them and therefore require
an external source [48]. The amino acids Lysine and Methionine are typically the
first amino acids to become limited within fish diets and are often supplemented in
fish feed, such as seen with most soy bean derived feed [45, 48].
17
22. Chapter 3 Alternative aquafeed considerations
Table 3.1: Overview of various fish feeds and relative protein content
Feed Source % Protein
content
Reference
fishmeal/oil 65-70% [47, 27]
Blood meal 90% [47]
Poultry bi-product meal 60% [27]
Meat and bone meal 51-65% [47, 27]
Feather meal 83-88% [47, 27]
Maize gluten 60% [27]
Soy meal 44-48% [47, 27]
Soy concentrate 65-76% [47, 27]
Canola meal 38% [47, 27]
Wheat gluten 70-80% [27]
Rapeseed concentrate 61% [27]
Periphyton meal - -
Lenseed - [47]
Hemp seed >50% [37]
Algae single cell meal - -
Insect meal 45-60% [16, 20]
In addition to protein, most carnivorous fish that represent the major consumption
of aquafeed in IFSs require an external source of highly unsaturated fatty acids
(HUFA). HUFAs are associated with dietary health in humans and can be described
structurally to have more than 4 double carbon bonds within a 20+ carbon chain [30,
48]. Also referred to as n-3 or Omega-3 fatty acids, HUFAs include eicosapentaenoic
acid (EPA), comprised of a 20 carbon chain backbone and docosahexaenoic acid
(DHA) comprised of a 22 carbon chain [47]. Both of these essential fatty acids
are derived from linoleic acid (LA), an 18 carbon chain precursor polyunsaturated
fatty acid (PUFA), also referred to as n-6 or Omega-6 fatty acid. While most fresh
water fish can elongate carbon chains and synthesize HUFAs, marine carnivorous
fish need to consume EPA and DHA [48]. This is the fundamental reason why
carnivorous marine species require more fishmeal and or fish oil in their diets in
comparison to fresh water species. It also highlights the challenge in locating the
proper replacement feed that has the appropriate protein and fatty acid profile.
In addition to meeting the above requirements, it is known that there is a high
variability between common ingredients used in fish feed depending on locations
and methods for producing aquafeed [24]. Glencross, Booth, and Allan 2007, discuss
variable content findings from a dozen different sources of lupin meal and protein
concentrates and argues for better quality standards in fish feed and oil production
18
23. 3.1 Fish Physiology
from manufacturers [24]. The following chapter discusses alternative aquafeeds on
a case by case basis followed by general methodologies that can be considered to
further increase efficiencies when using aquafeed.
19
24.
25. 4 Alternative aquafeeds available for
finfish aquaculture
4.1 Non pelagic fish, marine aquafeeds
4.1.1 Bycatch and trimmings
The FAO estimate that 6 million tons of trimmings from bycatch and harvested
aquatic organisms with the exception of algae is used in the production of fishmeal
and fish oil, making up 25% of fishmeal production in 2008 [1]. Tacon 1999, esti-
mated that 2 million tons of wild caught fish scraps were used in the production of
fishmeal and oil [50, 40]. Thus, the estimates for fish sourced bycatch inclusion in
aquafeed are between 2-6 million tons. If this is to become a tangible replacement
source of fishmeal and fish oil, processing facilities need to be in place in the areas
where bycatch occurs in significant volumes to make it economically feasible. It is
thought that the only places where bycatch and trimmings occur on a sizable scale
for processing is at West Dutch harbor and Kodiak harbor in Alaska [41].
4.1.1.1 Problems and pitfalls: Limited feed quality
Bycatch and processed trimmings often have a high bone content leading to ash
contents as high as 25% [27]. Fishmeal on the other hand has a ash content of roughly
14%, so the technique of deboning needs to be applied to bycatch and trimmings,
bringing the ash content down to as low as 7% [27]. This however means that less
than the entirety of bycatch and trimmings can be used and that bycatch has to go
through specialized processing. The problem of high ash content is also associated
with meat and bone meal (MBM) another alternative feed source mentioned later.
There are additionally two risks that need to be taken into account when considering
the use of bycatch and trimmings in fishmeal and oil production. The first is that
bycatch and trimmings are often low in protein but high in calcium, phosphorus,
and pollutants. This can lead to zinc deficiencies as well as bio accumulation of toxic
compounds such as Polychlorinated biphenyls (PCBs) and dioxins [41]. Secondly, if
we create incentives for bycatch, it lies directly counter to efforts of limiting bycatch
within the wild catch fishing industry.
21
26. Chapter 4 Alternative aquafeeds available for finfish aquaculture
4.1.1.2 Governance, solutions and future prospects: Importance of
monitoring
The use of bycatch in fishmeal and oil production is an appropriate waste pathway
for the waste stream of major and highly regulated fisheries, but should be closely
managed to prevent improper incentives to encourage increased hauls of bycatch.
The use of marine observers, remote monitoring devices attached to rear harvesting
areas of vessels, and strong governmental policies have allowed for better oversight in
both the United States and Canada. The use of bycatch therefore has the potential
to be responsibly integrated into fisheries within these areas. These monitoring sys-
tems still need to be encouraged in developing fisheries where monitoring is limited if
bycatch is to be responsibly used as an aquafeed source on a global scale. However,
the current amount of usable bycatch and efforts to reduce it in the future, mean it
will be limited in its overall ability to act as a significant source of aquafeed.
4.1.2 Krill
Another marine based feed and oil source being explored is krill. 118,124 tons of
Antarctic krill (Euphausia superba) destined for feed were landed in 2007 within the
Southern Ocean [1, 41]. This has since increased to just under 200,000 tons in 2011,
but remains under historic highs of close to 400,000 tons throughout the 1980’s and
early 90’s. Studies conducted on krill as an aquafeed supplement found that 20-60%
protein inclusion rates led to increased salmon growth when compared to controls
based on fishmeal diets [43]. The researchers attributed these findings to krill acting
as a feed attractant. Additionally, the amino acid and fatty acid profiles of the fish
were unchanged on a diet supplemented by krill [43]. Considering fish feed, wild fish
and krill represent the most natural fish diets with favorable amino acid and fatty
acid profiles but are questionable in their efficiency and overall sustainability.
4.1.2.1 Problems, governance, and future prospects: Fishing down the food
chain
There are major hurdles to overcome regarding krill harvesting including the high
distribution variability, distance to harvest, perishability, and potential serious ecosys-
tem impacts from harvesting from the base of the food web [41]. More importantly,
the krill feed industry as it stands has limited room to grow further. The commission
for the conservation of Antarctic marine living resources has set the catch limit in
2013 at 620,000 tons [2]. As there is little known of the current scale of dependance
that the Southern Ocean marine food web has on krill, I would argue the precau-
tionary approach in which krill harvest levels are maintained at a minimal level until
additional research on the implications of increasing harvests can be obtained.
22
27. 4.2 Terrestrial animals
4.2 Terrestrial animals
4.2.1 Blood meal, meat and bone, and poultry byproduct
The FAO estimated that the world produced 13 million tons of animal protein and
10.2 million tons of animal fat from meat and bone meal (MBM), blood meal, and
poultry by-product meal (PBM) in 2008 [1]. In addition to these 3 types of meals
there also exists feather meal, however MBM and PBM is thought to make up 80%
of all animal rendered feeds [27]. The United States alone produced 2.8 million tons
of animal rendered meal and a further 900,000 tons of PBM in 2000 [27]. Although
minimal, 5% of US production went to the pet food industry emphasizing alternative
feed pathways that the aquaculture industry has to compete with [27]. Terrestrial
animal rendered proteins are thought to have a more complete amino acid profile
than vegetable proteins and can be digestible by fish up to 80-90% [41]. The price has
also become more affordable as an alternative feed source with prices at $0.79/kg for
animal byproduct rendered meal versus $1.13/kg of anchovy fishmeal in 2009 [41].
In regards to using the entirety of an animal raised for consumption, the aquaculture
industry presents a solid solution for the use of the animal excess that would have
otherwise been thrown away. It may therefore be argued that this feed source could
be more sustainable because it originates from a waste stream rather than grown
with the single purpose of feed for aquaculture. Conversely, terrestrial animal rearing
is itself associated with a host of problems including excessive land degradation,
high feed requirements, and greenhouse gas production. Providing further economic
encouragement to this sector for its waste stream needs to therefore be taken into
account.
Some studies have recommended a fish replacement diet of less than 30% MBM
while others have been able to replace fishmeal with up to 75% PBM or MBM
before seeing negative effects [25, 9]. In relation to each other, PBM in one study
was found to have a FCR of 2.31 when it replaced 75% of the protein within the
diet of catfish, while MBM had a FCR of 3.14 when it replaced 75% of the dietary
protein [25]. This is most likely due to the fact that MBM has a higher ash content
[25]. In regards to rearing cobia, it was found that up to 50% of MBM or PBM could
be used without a negative effect, while 15% replacement yielded optimal growth
[57]. This shows us that animal rendered meals may be less effective than fishmeal
and fish oil diets and lead to higher FCRs when used as the main source of protein.
However, at low inclusion levels, animal rendered meal promotes growth with no
negative effects and can therefore play an important role in supplementing aquafeed
diets within the finfish aquaculture sector.
4.2.1.1 Problems and pitfalls: Variable replacement trials
We need to be critical of replacement aquafeed studies as most that measure the use
of animal rendered feed in the diets of fish, or crop derived feeds for that matter, also
23
28. Chapter 4 Alternative aquafeeds available for finfish aquaculture
include a host of other feed products. This is why “dietary protein” replacement was
specifically mentioned above rather than feed. Often studies will supplement either
fishmeal or fish oil with a new feed type, but not both as the other is maintained
within the test. Thus, by fully replacing fishmeal but still using significant fish
oil for all test subjects, scientists need to be cautious of saying they can rear fish
with a 100% fishmeal or fish oil replacement diet as it can be misleading. This
problem is further complicated by the additional incorporation of a host of other
food supplements including vitamins, minerals, crop derived proteins and fillers.
These additions are not minimal in their contribution as they often make up 50-75%
in weight of the test feeds [25, 57, 6]. This makes it extremely difficult to compare
studies when each experiment represents a fundamentally unique feed mix, especially
when as mentioned in chapter 3, the components themselves have been found to be
variable in content [24]. Attempts should be made by the scientific community to
work off dietary templates so that stepwise improvements can be made towards the
elimination of fishmeal and oil from aquafeed diets.
4.2.1.2 Governance and future prospects: Revisiting legislation
Many countries around the world already use animal rendered feed within their
aquaculture industry. Europe however, was an exception until the EU commission
lifted a ban that restricted the use of terrestrial animal rendered products as feed
for aquaculture at the beginning of this year, 2013. This allows the use of rendered
animal protein and fat as a viable source for aquafeed within the European Union
as of the 1st of June, 2013 [14]. One can therefore expect to see growth in this
sector over the coming years. Despite this international development, local Euro-
pean governance is also influencing the aquaculture industry and does not always
agree with European Union law. The UK for example, exhibits one of the highest
inclusion rates of fishmeal (36%) and fish oil (28%) in its aquafeed industry [53].
This is largely attributed to the strict standards that have been imposed by the
UK National Salmon Farming Association as well as retailers to ensure proper nu-
tritional qualities of healthy amino acids are maintained in fish for consumers [53].
If animal rendered meal as well as other replacement feeds are to play a role in
the conversion of the industry, it is vital that governmental agencies on all levels
communicate the merits and drawbacks of alternative feed sources so that they may
agree on common legislation, allowing the industry to move forward. This said, the
production volume of animal rendered feed and lifting of bans mean they will likely
continue to contribute a significant portion to overall aquafeed in the coming years.
4.3 Terrestrial Crops
Soy bean, corn, rapeseed, sunflower seed, flaxseed, wheat, hemp seed, and gluten
have all been used at varying degrees as a aquafeed source for finfish aquaculture [45].
24
29. 4.3 Terrestrial Crops
Others include canola, barley, cottonseed, and lupin [41]. One of the biggest issues in
using terrestrial plant based feed is creating feed that is low in fiber and starch, high
in protein content, has a desired amino acid profile, palatable for fish consumption,
and easily digestible [41]. One concern regarding vegetarian sources of protein is the
difficulty to break down phytic acid, which acts as a storage molecule of phosphorus
in seeds. The enzyme Phytase that most fish lack, helps to break down phytic acid
and is only naturally occurring in grazing fish [45, 12]. Other important enzymes
include endo-xylanase, responsible for the break down of fiber and carbohydrates
and protease for animal rendered feed which hydrolyzes connective tissues and skin
[27]. These enzymes often have to be incorporated with these aquafeeds, particularly
those of terrestrial crop origin. Therefore total digestibility of terrestrial based feed
rarely exceeds 50% [12].
4.3.0.3 Problems and pitfalls: Limited land and fresh water
The major concern with using crop based feeds is the land area and fresh water
that is required to grow them. The land use for production of major crops included
in aquafeed can be observed in Tab. 4.1. Producing food destined to feed other
animals will never be as sustainable or efficient as consuming that food directly.
Land use for feed also competes with wild life habitat, livable space, and other
product production such as biofuels. Additionally 70% of usable water is currently
destined for agricultural practices where globally, 40% of the world’s population is
thought to be in a severe water stressed area [23].
Table 4.1: Crop production and land area usage. [19]
Crop Land use
area (ha)
Yield
(tons/ha) Production
(million
ton)
Processed
oil
(million
tons)
Maize 170.4 M ha 5.1847 883.4 MT 2.3 MT
Wheat 220 M ha 3.1948 704.1 MT gluten
Palm oil ? ? ? 48.6 MT
Soy Bean 103 M ha 2.5333 260.9 MT 41.6 MT
Barley 48.6 M ha 2.7627 134.3 MT -
Cottonseed 35 M ha 2.1947 77.3 MT 5 MT
Rapeseed 33.6 M ha 1.8563 62.4 MT 22.3 MT
Sunflower seed 26 M ha 1.5434 40.2 MT 13.3 MT
Linseed 2 M ha 0.7833 1.6 MT 520,929
Lupin 959,099 1.1545 1.1 MT -
Hemp seed 27,038 3.2969 89,142 -
25
30. Chapter 4 Alternative aquafeeds available for finfish aquaculture
Furthermore, the use of crops present a unique set of challenges when replacing fish
oil. Multiple experiments have been carried out in an attempt to replace fish oils
with crop based oils such as palm and rapeseed oil. The replacement of oils present
a problem as vegetable oils are high in saturated fatty acids. Although 100% oil
replacement can be achieved without visible negative effects of FCRs or fish growth,
it was found that as palm oil increased in the inclusion of Atlantic salmon diets, the
total saturated fatty acids increased linearly, replacing healthy highly unsaturated
fatty acids typically found within salmon [6]. Palm oil replacement above 50% was
found to significantly reduce these essential fatty acids leading Bell et al. 2001, to
argue the use of palm oil during the grow out stage of fish production and prior
to a finishing feed [6]. Similar results were noted for the use of Rapeseed oil in
Atlantic salmon [7]. It has been found that there is some evidence of fatty acid
turnover and metabolism occurring in fish fed initially with vegetable oils, followed
by a finishing feed of fishmeal. This supports the methodology of initially using crop
based feeds followed by fishmeal and fish oil based feeds to obtain a suitable fatty acid
profile while reducing overall fishmeal and fish oil consumption [30, 41]. It should be
noted that in both of these palm and rapeseed oil substitution experiments, fishmeal
inclusion in the diet was maintained above 50%, highlighting the pitfall mentioned
in the previous section of working with either fishmeal or fish oil, but not both
simultaneously [6, 7].
4.3.0.4 Governance and future prospects: Widespread use
Despite the land, water and dietary problems, crop inclusion in aquafeed is still
significant [37, 27]. Additionally, production of these crops occurs at the base of
the food chain and on such a large scale Tab. 4.1, that their role in the future of
aquaculture is almost guaranteed. Of crops being used and investigated, soy bean is
the most widely used within aquafeed [1]. I will therefore briefly discuss it specifically
amongst other crops within the following section. It should be noted however from
Tab. 4.1, that maize, wheat, palm, and barley also have huge areas of land dedicated
to their production. These are in turn associated with massive yields and although
not included in aquafeed on the scale of soy bean, may never the less contribute to
the future of aquafeeds.
4.3.1 Soy bean
The world production of soybean destined for aquaculture feed was 6.8 million tons
in 2008, or 23.2% of total aquafeed by weight [1]. Chou et al. 2004, found in studies
on the salt water carnivorous fish cobia, that supplementing diets with soybean over
50% caused detrimental effects, but encouraged optimal fish growth when included
at 17% [13]. The inclusion rate of soybean meal varies depending on the fish type.
26
31. 4.3 Terrestrial Crops
Blue catfish can handle up to 70% defatted soybean in their diet [56], while catfish
meal within the United States is comprised of 45-50% soybean [27]. Conversely, rain-
bow trout experience detrimental effects above 20% defatted soybean [33]. Known
fish types and the possible inclusion of soybean within their diets can be found in
Tab. 4.2. Additionally, companies like Monsanto have begun to engineer soy bean
to generate stearidonic acid, an Omega-3 fatty acid precursor [47]. This may allow
for higher inclusion rates within aquafeeds over the coming years as well as diminish
the demand for fish oil as fish are increasingly able to obtain essential fatty acids
from soy bean.
Table 4.2: Defatted soybean inclusion in fish diets. Adapted from Chou et al. 2004.
[13]
Fish type % of soybean that can be included in fish diet Reference
Blue catfish 70% [56]
Rainbow trout <20% [33]
Atlantic salmon <25% [33]
Cobia 40% [37]
4.3.1.1 Problems and pitfalls: Digestibility
One of the major problems associated with soybean and other seed sources used as
feed in finfish aquaculture is the presence of protease inhibitors within the plant.
These are enzymes that block the activity of trypsin enzymes secreted by the di-
gestive system of fish [13]. These inhibitors can be broken down by steaming the
soybean in toasters during oil extraction. This does not completely break down
the inhibitors and may contribute to the negative impact soybean has been found
to have on salmon fry. Hardy 2000, found that the inclusion of just 5% soybean
within salmon fry diet led to reduced food intake [27]. This highlights a difficulty of
working on fish with variable feed requirements at various stages of their life cycle.
Additionally, as mentioned above for other crops, land and water allocation are of
serious concern as the world currently has 103 million hectares of land devoted to
the production of soy bean (Tab. 4.1).
4.3.1.2 Governance and future prospects: A role for soy
Soy bean already makes up a huge component of aquafeed and as such will certainly
play a role in the future of aquafeed, especially as enriched Omega-3 soy bean comes
on the market. I would argue that using soy bean is better than using fishmeal
or fish oil to grow fish, but that other alternatives show even more potential when
considering overall sustainability as an alternative aquafeed. Soy bean should act
as a filler but should not act as a single solution in regards to developing a truly
sustainable aquafeed.
27
32. Chapter 4 Alternative aquafeeds available for finfish aquaculture
4.3.2 Periphyton
Periphyton is the build up of aquatic plants, animals, and associated fauna on
aquatic surfaces [55]. It is thought that upwards of 50% is non-algae in origin as
bacteria and microbes add to this intricate community, creating a matrix high in
organic matter [55]. Periphyton can be consumed by many fish such as carp and
tilapia, as well as catfish [55]. Humans have taken advantage of this by adding
substrates to lakes and lagoons with the highest success in the form of bamboo
poles over PVC piping and sugarcane, although other available surfaces can be used
[55, 36]. Providing this substrate increases the surface area for periphyton growth
which is dependent on nutrients, light, and substrate availability [55]. Generally,
these structural additions are referred to as “brush parks”. The use of periphyton
for fish feed is long practiced in mostly developing nations including Bangladesh,
Cambodia, China, Ecuador, India, Madagascar, and Sri Lanka [32]. Particularly
successful fish reared using periphyton include Labeo rohita and Tor khudree; two
species of carp [34]. Through various studies, it was found that the use of brush
parks can double the yield of fish reared in ponds with no supplemental feeding
[5, 35]. However, it may take multiple days to remove a brush park during fish
harvests thereby limiting the technique to smaller stakeholders operating within
EFSs and SIFSs [55]. Van Dam et al. 2003, found that brush parks on average yield
5 tons/ha/yr, making them a viable opportunity for local actors [55].
4.3.2.1 Problems and pitfalls: Limited to local actors
Potential negative impacts associated with using brush parks are deforestation, eu-
trophication as the brush park breaks down, and erosion if the park is built from
surround mangroves [55]. Additionally, the literature suggests that although inclu-
sion of a brush park may improve fish yields, there is not a linear relationship. Thus,
brush parks will only improve a system to a point whereby adding additional bam-
boo does not correlate to higher fish yields. The density at which optimum returns
occurred for Keshavanath et al. 2004, was roughly 4 poles per m2
, although their
next treatment was 8 poles per m2
and they urge additional fine tuning within their
study [34]. The use of brush parks is further limited to specific species that may not
be in as high demand as carnivorous species and therefore restricted to local actors.
4.3.2.2 Governance and future prospects: A local solution
Brush parks are a prime example of implementations that local actors involved with
EFSs and SIFSs can take without making major investments. Bamboo is one of
the quickest growing species in the world and happens to grow in many parts of
Asia where EFSs and SIFSs are common. In the attempt to curb fish farmers from
moving towards the use of manufactured aquafeeds and becoming IFSs, the practice
of using bamboo to grow periphyton should be encouraged by local governments and
28
33. 4.4 Innovative aquafeeds
stakeholders alike, so that farmers can increase yields while resisting the conversion
to IFSs.
4.4 Innovative aquafeeds
4.4.1 Single celled organisms (SCO)
There has been a great deal of research as of late into single celled organisms (SCO)
and their ability to produce biofuels, lactic acid for pharmaceuticals or detergents,
as well as the possibility to make feeds or favorable dietary oils with HUFAs. One
example of SCO used in fish feed are thraustochytrids. These are large-celled marine
heterokonts classified as oleaginous or “oil producing” microorganisms due to their
production of long chain fatty acids [11]. These organisms have been successfully
used in trials as feed in the grow-out phase of Atlantic salmon [41, 11]. Another
study harvested single celled artemia and rotifer hetertrophes after feeding single
celled algae to them. They were able to produce feed found suitable for early fish
larvae grow out stages at a cost of $5 per kg or ~$4,500 per ton [28, 3]. This is
in stark contrast to the cost of fish oil or fishmeal as it is roughly 3 times more
expensive, but with continual research and innovation, the price is likely to come
down allowing SCOs to become a viable option for fish feed in the future.
4.4.1.1 Problems and pitfalls: In its infancy
The SCO feed industry is still in the development stage and therefore requires ad-
ditional funding, research, and support from knowledge centers and governments
alike. Dr. Arjen Roem, a leading scientist on aquafeed development at Wageningen
University, discussed how SCOs and algae showed the most potential for replacing
the use of fish oil within the aquafeed industry and highlighted that this is currently
the focus of much of the scientific community concerned with aquaculture [47]. This
is in large part due to the fact that there are limited suitable replacements for fish
oil, whereas fishmeal is already being replaced by multiple alternative feed types.
4.4.1.2 Governance and future prospects: A sustainable feed source
If the SCO feed market can merge with the biofuel market at the research and
development stage, it is thought that there is a better chance for SCO to become
cost effective and a viable source of aquafeed in the near future [41]. Fish oil is set
to increase in demand as people seek it out for direct consumption based on health
benefits, along with an ever growing aquaculture industry. These trends will further
generate the need for replacement oils and likely drive the development of SCOs.
This has already been observed in aquafeed composition based on recent price hikes
29
34. Chapter 4 Alternative aquafeeds available for finfish aquaculture
in fishmeal and fish oil over the last two decades and with a global aquaculture
industry valued at $119 Billion in 2010, this trend will likely continue to drive
innovation in the aquafeed sector [1]. Since there is the potential to grow SCOs in
marine waters, two significant implications can be drawn. One is that SCOs require
no fresh water, a commodity already increasingly becoming scarce. The second is
that SCOs do not require terrestrial land space for growth. With SCOs rapid ability
to grow and replicate, SCOs present significant advantages when considering overall
sustainability and efficiency in comparison to other aquafeeds and their success will
be dependent on bringing down the cost of production.
4.4.2 Insects
The use of defatted maggot meal was successful when fed to the catfish Clarias
gariepinus. With a crude protein content of 45.6%, no significant differences were
found when substituted for fishmeal, although cod oil was included within all dietary
treatments [20]. In another study, the use of house fly larvae was studied as a feed
source within broiler chickens. It was found that Musca domestica had a dried crude
protein content of 60%, a similar amino acid profile to fishmeal, and no difference
in growth was observed when fishmeal was substituted for the insect meal in broiler
diets [16]. This has a potential significant impact on the finfish aquaculture sector
as the poultry and swine industries represent an overall significant consumption of
the 7.74 million tons of pelagic fish not destined for aquafeed [40]. If insects can be
used to replace fishmeal within these other industries, it indirectly may reduce the
pressure on capture fisheries and the demand for fishmeal and fish oil. Additionally,
similar protein content and nutritional profiles of insect meal in regards to fishmeal
will allow for the continual development of insect use in aquafeed itself.
4.4.2.1 Problems and pitfalls: New industry
The use of insects as fish feed has huge potentials, but is currently still in its infancy
in regards to use on an industrial scale. The ban on the use of animal rendered
products as feed within the EU was lifted this year as of June 1st, 2013 as mentioned
earlier [14]. The use of processed animal proteins has been banned in the EU since
2001 with the outbreak of mad cow disease, but with new legislation, we will likely
see growth in this sector over the coming years. Insects do however need to be
turned into meal prior to feeding to fish. It is thought this avoids the spread of
disease, reduces bacteria as well as algae blooms, and overall decreases the chance
of fish mortality [20]. This does add to processing costs making it more expensive
to bring to market, setting it on par with other feed manufacturing processes.
30
35. 4.4 Innovative aquafeeds
4.4.2.2 Governance and future prospects: Using waste
The amount of compostable waste exiting cities is staggering. The journal of me-
chanical engineers put the amount of global food waste equivalent to 1.3 billion tons
a year from farm to fork [22]. If municipalities were able to sort their biodegradable
waste and use it as a feed source for insects, it would help to close a major energy
cycle as a significant waste stream becomes the input of a sustainably grown fish
feed. If food waste is to be used as a feed source within the EU, regulation often
requires that it is heat treated [47]. Given the fact that fish feed is changing rapidly
in composition from fishmeal and fish oil to alternative protein sources, it would be
advantages to promote this sector further as it stems from food waste while other
fishmeal sources such as crops depend on the designation and use of land and water
to grow feed.
31
36.
37. 5 Efficiency through rearing and
feeding methodology
Thus far, various fish feeds have been discussed to highlight the current status of
the aquaculture feed industry, specific problems associated with each aquafeed type,
and future prospects for those feeds. However, if the focus of this paper concerns
efficiency of feeds, the methods in which fish are raised as well as how feed is delivered
needs to be discussed. This may give a more complete picture of feed within the
finfish aquaculture industry and viable pathways forward towards making the finfish
feed industry more efficient.
5.1 Preventing aquafeed waste
Cho and Bureau 2001, found that feed waste within the aquaculture industry de-
pends mostly on practices rather than feed itself [12]. It is thought that up to 10%
of fish feed is wasted due to the fact it is not ingested by fish during feeding [48].
This stems from diet selection, using accurate growth predictions, waste estimation,
ration allowance, and the feeding strategy used [12]. Fish farms rely on oil and feed
manufacturer charts and scientific publications to make decisions about the amount
of feed, method, and type of feed they consider to be best for their stocks. It is
therefore important to continually investigate best practices and convey scientific
results to fish farmers, if progress is to be made on efficiency of feed in aquaculture
[12].
Craig and Helfrich 2009, deliver specific recommendations regarding simple steps to
reduce feed waste. Industrial fish feed typically comes in 50 Ibs. sacks and should
be stored out of the sun in the shade at cool temperatures for no more than 100
days, and sacks should not be stacked more than 10 high [48]. They go further to
suggest that farmers should avoid feeding fish in stagnant water during the early
mornings when oxygen levels are lower as it is associated with decreased fish activity
[48]. Additionally, they show how size and weight of fish play a role in the fishes
ability to digest the meal as well as the pellet size of the meal itself [38, 24, 46].
These recommendations may seem trivial, but have huge implications on efficiency
of feed use and therefore important when we consider the entirety of efficiency within
aquaculture.
33
38. Chapter 5 Efficiency through rearing and feeding methodology
5.2 Innovative feeding methods
For most fish, 95% of the total aquafeed consumed over the life span of the fish occurs
during the juvenile and grow out stage [41]. Using finishing feed is a innovative
method in which fish farmers will give fish a more natural fish feed diet during the
final 18-24 months before harvesting after having grown the fish on alternative crop
based feeds. This is thought to decrease the total use of fish oil by up to 85% when
compared to fish raised completely on a fish based diet [45]. The finishing feed has a
dilution effect, depositing desired fatty acids within the final life stage of the fish so
that the fatty acid profile is comparable to fish raised on a fishmeal based diet [30].
This innovative feeding methodology yields insight that timing and methodology
are equally important when considering efforts to using feeds more efficiently.
5.2.1 Polyculture
Another way to promote efficiencies that is attracting attention is raising fish yields
by growing multiple species together in what has been termed polyculture. Polycul-
ture involves using as many food and waste streams as possible by incorporating fish
with distinct niches such as surface water fish, pelagic, and benthic species within
the same pens or ponds [51]. The beginning of fish polyculture has been traced
back to the Chinese Tang Dynasty, 7th century and is defined as growing two or
more species within the same environment [58, 51]. An example of this is the use
of carp in fresh water systems. The silver carp acts as a plankton feeder, the grass
carp as a herbivore of macrophytes, the common carp as an omnivore of detritus
on the bottom and the bighead carp as a zooplankton filter feeder [40, 51]. Bottom
feeders are thought to promote phosphorus cycling as they turbate the benthic envi-
ronment, which can make it unnecessary to provide external fertilization [39]. Most
polyculture is based on EFSs where no external feed is added. However, polyculture
can extend to salt water environments where shellfish and seaweeds can be raised on
the effluent from salmon, thereby increasing aquaculture production while limiting
waste streams that leach into the surrounding environment [40, 31, 42].
The implications of expanding polyculture with existing infrastructure are major,
especially when considering the Asian rice paddy system where juvenile carp are
introduced when sewing of the rice. The FAO estimated that globally, 164 million
hectares of land are used for the production of rice within paddy systems [19]. They
further estimate that China uses 15% of its land, or 1.3 million hectares of total rice
paddy devoted land in conjunction with fish production which annually yields 1.2
million tons of fish and other animals [1]. The FAO suggests that implementing this
polyculture system on rice paddies leads to a 68% reduction in the use of pesticides,
24% less fertilizer is required as the fish excrete it as waste, 30% lower methane
emissions are produced and an increase of 400% in profit is realized for the farmer
[1]. Based on the FAO estimates, if all rice production was done in conjunction
34
39. 5.2 Innovative feeding methods
with fish production, it would yield roughly 150 million tons of additional fish and
other aquatic animals every year. This is one example of how polyculture can lead
to increased efficiencies and profits for all stake holders involved.
There is a critical role for government to play within the promotion of polyculture
and it should begin by making aquafarms responsible for their waste production.
IFS waste streams are largely not included in the cost for fish farmers and until they
are, there remains no pressure for farmers to deal with effluent from fish farms. Fish
can excrete up to 50% of the protein they consume as waste, mostly as ammonia
through the gills, where an additional 10% exits as solid waste [48]. Goldburg and
Naylor 2005, estimated that a kilogram of salmon release 0.02-0.03 kg of nitrogen
per year [26]. By taking the average American’s annual production of nitrogen waste
and the National Oceanic and Atmospheric Administration (NOAA) goal of having
a $5 Billion dollar aquaculture industry within the United States by 2025, they were
able to calculate that this would result in a nitrogen output equivalent to 17.1 million
people’s untreated sewage waste entering into coastal waters each year [26]. This
problem is compounded as IFSs often cluster together along coastlines to benefit
from the economy of scale [26]. But there are signs of a changing time. In Denmark,
the cost of remediating 1 kg of nitrogen is equivalent to $44 [42]. By coupling the
true costs of fish production with waste through governmental legislation, farmers
would be led to limit their transition from EFSs to IFSs, while encouraged to limit
waste by seeking out possible polyculture implementation and solutions.
35
40.
41. 6 Discussion and Conclusion
The fact of the matter is that the aquaculture industry is rapidly growing and
changing, in some ways for the better and others for the worse. The global industry
is shifting towards IFSs which is fundamentally the wrong direction. EFSs need to
be promoted wherever possible and government has a role to play in making sure
the true costs of IFSs are realized by charging farmers for their waste. In doing
so, IFSs are more likely to incorporate efficient process and methods to maintain
and increase profitability wherever possible. With proper regulation, government
also has a responsibility to become more clear in their governance of aquaculture so
that the industry can better operate with less bureaucracy. Difficulties in legislation
can be highlighted within the US where there are no formal policies to manage
aquaculture, but 32 state programs with over 1200 state laws that impact various
facets of the industry [15]. This chocks the industry’s ability to operate and move
forward as the science recommends it to do.
In regards specifically to feed, the industries inclusion of fishmeal and fish oil are
on the decline. Fishmeal destined for salmon feed has been reduced from inclusion
levels of 45-50% 20 years ago to 10-15% today and it is thought that the industry
could become completely independent in the coming decade [47]. Fish oil is thought
to be more critical within the diets of fish due to essential dietary components
and therefore a harder ingredient to replace. But reductions in this too are being
observed, from 19.7% inclusion within European aquafeed 20 years ago to less than
10% today [47]. Therefore, the current challenge within the industry is the work
towards the developments of efficient and sustainable feeds, as well as oils that have
the same nutritional value as fish oil and can therefore replace it altogether. If one
looks at various aquafeed costs in the year 2000, the market is clearly driven by
specific feed sources (Tab. 6.1).
37
42. Chapter 6 Discussion and Conclusion
Table 6.1: Cost of feed per ton in year 2000 within the US [27]
One can see that back in 2000, anchovy meal was low compared to the $1,500 per
ton in 2010, which made it a likely choice for the aquafeed industry at the time. The
cost of animal rendered feed is still low and therefore will likely continue to grow as
a aquafeed source, especially as meat production increases. While crop production
is thought to increase proportionally to population growth, meat consumption will
increase by 22% per capital between 2000 and 2030 [8]. The price of crops will also
increase as demand for direct consumption and feed for livestock grows. This poses
a risk as aquafeed sources including corn, soybean, and canola are very low in price
per ton now and therefore attractive, but unlikely to provide a sustainable source
for aquafeed in the coming years.
I believe the more sustainable sources of feed lie in highly managed by-catch, insects,
SCOs for oils, and excess animal rendered feeds, although there are risks and chal-
lenges to overcome for each of these feed sources from creating improper incentives
to additional needed research. A overview of each feed source and its overall effi-
ciency can be seen in Tab. 6.2. Feed generated from krill, I believe posses the same
environmental risk that fishmeal and fish oil based feeds pose and therefore should
be avoided to maintain Southern Ocean ecosystem resilience. Feed originating from
crops has a role to play in aquafeed, but it should be minimized to filling in the
gaps, secondary to these other feed sources originating from waste streams. SCOs
are an exception as their potential to be grown without the need of fresh water or
extensive agricultural land is favorable.
38
43. Discussion and Conclusion
Table 6.2: Overview of efficiency of aquafeeds
Feed type Current
use
Level of
sustain-
ability
Points to consider
Wild
catch, krill
fully
exploited
0 Inefficient, risk to ecosystem if
expanded, could directly be
consumed
Terrestrial
crops
growing * Extensive land and water use,
crops could directly be
consumed.
Bycatch limited
growth left
** Waste origin, limited by
processing facilities, negative
incentive to increase bycatch.
Animal
rendered
growing ** Waste origin, large footprint for
terrestrial animals, negative
incentive to increase meat
production.
Periphyton localized *** Limited to EFS and SIFS, labor
intensive, should be promoted
when possible.
SCO future
prospec-
tive
*** Grown in salt water, no land
needed, R&D required to
develop.
Insects future
prospec-
tive
*** Food waste stream origin, water
needed, R&D required to
develop.
0- The least sustainable feed used to grow fish *-Potential for inclusion in aquafeed
but should be avoided when possible **-Derived from waste stream, but has
potential to create negative incentives within other industry ***-Derived from
waste streams or requires no limiting resources with limited negative impact on
other industry.
Scientists need to start standardizing their experiments to create a foundation in
which feed substitution experiments can progress. The current incorporation of
a multitude of feed components with variable fishmeal and or fish oil slows the
scientific progression, especially when it is carried out over a multitude of fish species.
Every effort needs to be made to communicate with aquafeed producers, allowing
for stepwise improvements to achieve sustainably sourced aquafeeds. If one looks at
the salmon feed industry, there are three major feed manufacturers representing over
90% of the salmon feed market. They include Skretting based out of the Netherlands,
39
44. Chapter 6 Discussion and Conclusion
Ewos based in Norway, and Biomar based in Denmark [47]. By communicating
with these companies and organizing research to stem from a common foundation,
progressive changes in farmed salmon diets will be more quickly realized.
This being said, the use of fishmeal and oil in aquaculture should come to an end.
The multitude of efficiently sourced aquafeeds that can be substituted for fishmeal
and fish oil, without negative impacts on the health and growth of fish are numerous.
Additionally, while there is a current emphasis placed on feed resource sustainability,
there exist minimal debate on whether pelagic fish should be redirected for direct
human consumption [54]. As techniques improve to allow more people to eat smaller
pelagic forage fish, there is the opportunity to feed a larger number of people when
compared to the fish raised on fishmeal and fish oil. This idea is based on the prin-
ciple of energy conservation per trophic level, and although variable, is commonly
accepted that 10% of energy is conserved with each higher trophic level [44]. This
means we could potentially feed 10 times the number of people on a small pelagic
fish diet when compared to salmon or other higher trophic level species.
As the finfish aquaculture industry continues to be negatively observed within the
public eye as inefficient, unsustainable, and behind the times, adopting more efficient
aquafeeds could also give the industry a much needed boost in public opinion. A
recent story on the British Broadcasting Company highlights the problem as recent
plans were announced to set up a salmon farm near the islands of Aran off Ireland,
estimated to produce 15,000 tons of salmon per year with a standing salmon stock
of 7 million fish [21]. The article discusses stiff opposition to the plans from local
residents and anglers which provides insight into how public perception is continu-
ally hindering growth of the aquaculture industry. By sustainably sourcing finfish
aquafeed, the industry has a real chance to address the lack of efficiencies and waste,
and begin the process of being viewed in a more positive light.
Lastly, significant changes within the aquaculture industry will continue to occur
based on the consumer choices and spending. By eating smaller herbivorous fish,
we create the demand for change from higher trophic level carnivorous fish. We
also have the potential to collectively demand sustainably raised carnivorous fish.
As scientists, I believe our role extends beyond consumers as the task falls to us to
translate our scientific findings and get it into the hands of the consumer so that
they have the opportunity to make informed decisions. Through communication,
continual innovation, and action, the opportunity to improve the efficiency and
overall sustainability of the finfish aquaculture industry is tangibly within reach.
40
45. Acknowledgments
I would like to thank Dr. Jasper de Goeij from the University of Amsterdam for the
supervision of this project, providing feedback and direction throughout the process.
I would additionally like to thank Dr. Harm van der Geest for his feedback moment
and for taking the time to act as examiner for this project. Lastly, I would like to
thank Dr Arjen Roem from Wageningen University for his time and willingness to
share his extensive insight and knowledge concerning the aquaculture industry.
41
46.
47. Bibliography
[1] Fao fisheries & aquaculture department. the state of world fisheries and aqua-
culture. food and agriculture organization of the united nations, 2012.
[2] Commission for the conservation of antarctic marine living resources
(ccamlr). krill fisheries. po box 213, north hobart 7002, tasmania, australia.
http://www.ccamlr.org/en/fisheries/krill-fisheries. accessed 5-8-2013. Online,
August 2013.
[3] Naser Agh and Patrick Sorgeloos, editors. Handbook of protocols and guidelines
for culture and enrichment of live food for use in larviculture. Artemia and
Aquatic Animals Research Center, 2005.
[4] Anon. Fish food in the chilean salmon: conversion rates. Association of Chilean
salmon industry, 1:1–8, 2006.
[5] M. E. Azim, M. A. Wahab, A. A. van Dam., M. C. M. Beveridge, and M. C. J.
Verdegem. The potential of periphyton-based culture of two indian major carps,
rohu labeo rohita and gonia labeo gonius. Aquaculture research and develop-
ment, 32:209–216, 2001.
[6] J. G. Bell, R. J. Henderson, D. R. Tocher, F. McGhee, J. R. Dick, A. Porter,
R. P. Smullen, and J. R. Sargent. Substituting fish oil with crude palm oil in
the diet of atlantic salmon (salmo salar), affects muscle fatty acid composition
and hepatic fatty acid metabolism. The Journal of Nutrition, pages 222–230,
2001.
[7] J. G. Bell, J. McEvoy, D. R. Tocher, F. McGhee, P. J. Campbell, and J. R. Sar-
gent. Replacement of fish oil with rapeseed oil in diets of atlantic salmon (salmo
salar), affects tissue lipid compositions and hepatocyte fatty acid metabolism.
The Journal of Nutrition, pages 1535–1543, 2001.
[8] S. Bringezu, H. Schutz, M. O’ Brien, L. Kauppi, R. W. Howarth, and J. Mc-
Neely. Assessing biofuels. Technical report, (UNEP) United Nations Environ-
ment Programme, 2009.
[9] D. P. Bureau, A. M. Harris, and C. Y. Cho. Feather meal and bone meals
from different orgins as protein sources in rainbow trout, oncorhynchus mykiss.
Aquaculture, 181:281–291, 2000.
[10] J. C. Callaway. Hempseed as a nutritional resource. an overview. Euphytica,
140:65–72, 2004.
43
48. Bibliography
[11] C. G. Carter, M. P. Bransden, T. E. Lewis, and P. D. Nichols. Potential of
thraustochytrids to partially replace fish oil in atlantic salmon feeds. Marine
biotechnology, 5:480–492, 2003.
[12] C. Y. Cho and D. P. Bureau. A review of diet formulation strategies and
feeding systems to reduce excretory and feed wastes in aquaculture. Aquaculture
Research, 32 (Suppl. 1):349–360, 2001.
[13] R. L. Choua, B. Y. Hera, M. S. Sua, G. Hwangb, Y. H. Wub, and H. Y. Chenb.
Substituting fish meal with soybean meal in diets of juvenile cobia rachycentron
canadum. Aquaculture, 229:325–333, 2004.
[14] EU Commision. Eu commision regulation. Official journal of the European
Union, 56:1–14, 2013.
[15] M. R. DeVoe and C. E. Hodges. Responsible Marine Aquaculture. CABI Pub-
lishing, 2002.
[16] M. Dordevic, B. Radenkovic-Damnjanovic, M. Vucinic, M. Baltic, R. Teodor-
ovic, L. Jankovic, M. Vukasinovic, and M. Rajkovic. Eeffect of substitution
of fish meal with fresh dehydrated larvae of the house fly musca domestica,
on productive performance and health of broilers. Acta Veterinaria (Beograd),
54:4:357–368, 2008.
[17] P. Edwards. Environmental issues in integrated agriculture-aquaculture and
wastewater-fed fish culture systems. Environment and aquaculture in developing
countries, 31:139–170, 1993.
[18] FAO. Fao fisheries department, fishery information, data and statistics unit.
fishstat plus. universal software for fishery statistical time series. aquaculture
production quantities 1950-2006., 2008.
[19] FAO. Food and agriculture organization of the united nations. faostat., 2011.
[20] E. A. Fasakin, A. M. Balogun, and O. O. Ajayi. Evaluation of full-fat and defat-
ted maggot meals in the feeding of clariid catfish clarias gariepinus fingerlings.
Aquaculture Research, 34:733–738, 2003.
[21] D. Fleming. Bbc. irish battle over plans for aran giant salmon farm. accessed
8-6-2013. http://www.bbc.co.uk/news/world-europe-23550159. online, 8 2013.
[22] Dr. T. Fox and C. Fimeche. Global food, waste not, want not. Institute for Me-
chanical Engineers, 1 Birdcage Walk, Westminster London SW1H 9JJ, January
2013.
[23] G20. Sustainable agricultural productivity growth and bridging the gap for
small-family farms; with contributions by bioversity, cgiar consortium, fao, ifad,
ifpri, iica, oecd, unctad, coordination team of un high level task force on the
food security crisis, wfp, world bank, and wto. Technical report, Interagency
Report to the Mexican G20 Presidency, 2012.
44
49. Bibliography
[24] B.D. Glencross, M. Booth, and G.L. Allan. A feed is only as good as its
ingredients - a review of ingredient evaluation strategies for aquaculture feeds.
Aquaculture Nutrition, 13:17–34, 2007.
[25] A. M. Goda, E. R. El-Haroun, and M A Kabir Chowdhury. Effect of totally or
partially replacing fish meal by alternative protein sources on growth of african
catfish clarias gariepinus (burchell, 1822) reared in concrete tanks. Aquaculture
Research, 38:279–287, 2007.
[26] R. Goldburg and R. Naylor. Future seascapes, fishing, and fish farming. Fron-
tiers in Ecology and the Environment, 3:21–28, 2005.
[27] R. W. Hardy. New developments in aquatic feed ingredients, and potential of
enzyme supplements. Hagerman Fish Culture Experiment Station, University
of Idaho., pages 216–226, 2000.
[28] M. Harel, W. Koven, I. Lein, Y. Bar, P. Behrens, J. Stubblefield, Y. Zohar,
and A. R. Place. Advanced dha, epa, and ara enrichment materials for marine
aquaculture using single cell heterotrophs. Aquaculture, 213:347–362, 2002.
[29] A. Jackson. Fish in - fish out (fifo) ratios explained. Aquaculture Europe, 34:3,
2009.
[30] M. Jobling. Finishing feeds for carnivorous fish and the fatty acid dilution
model. Aquaculture Research, 35:706–709, 2004.
[31] T. O. Jones and G. K. Iwama. Polyculture of the pacifc oyster, crassostrea
gigas, with chinook salmon, oncorhynchus tshawytscha. Aquaculture, 92:313–
322, 1991.
[32] J. Kapetsky. Brush park fisheries. some consideration for the management of
coastal lagoon and estuarine fisheries. FAO fisheries technical paper, 218:18–28,
1981.
[33] S. J. Kaushik, J. P. Cravedi, J. P. Lalles, J. Sumpter, B. Fauconneau, and
M Laroche. Partial or total replreplace of fish meal by soybean protein on
growth, protein utilization, potential estrogenic or antigenic effects, choles-
terolemia and flesh quality in rainbow trout, oncorhynchus mykiss. Aquaculture,
133:257–274, 1995.
[34] P. Keshavanath, B. Gangadhar, T. J. Ramesh, A. A. van Dam, M. C. M. Bev-
eridge, and M. C. J. Verdegem. Effect of bamboo substrate and supplemental
feeding on growth and production of hybrid red tilapia fingerlings. Aquaculture,
235:303–314, 2004.
[35] P. Keshavanath, B. Gangadhar, T. J. Ramesh, A.A. van Dam, M. C. M. Bev-
eridge, and M. C. J. Verdegem. The effect of periphyton and supplemental
feeding on the production of the indigenous carps torkhudree and labe fimbria-
tus. Aquaculture, 213:207–218, 2002.
[36] P. Keshavanath, B. Gangadhar, T. J. Ramesh, J. M. van Rooij, M. C. M.
Beveridge, D. J. Baird, M. C. J. Verdegem, and A. A. van Dam. Use of artificial
45
50. Bibliography
ssubstrate to enhance production of freshwater herbivorous fish in pond culture.
Aquaculture Research, 32:189–197, 2001.
[37] A. N. Lunger, E. McLean, and S.R. Craig. The effects of organic protein
supplementation upon growth, feed conversion and texture quality parameters
of juvenile cobia (rachycentron canadum). Aquaculture, 264:342–352, 2007.
[38] I. Lupatsch, G. W. Kissil, and D. Sklan. Comparison of energy and protein
efficiency among three fish species, sparus aurata, dicentrarchus labrax, and
epinephelus aeneus. energy expenditure for protein and lipid deposition. Aqua-
culture, 225:175–189, 2002.
[39] A. Milstein, M. E. Azim, M. A. Wahab, and M. C. J. Verdegem. The effects
of periphyton, fish and fertilizer dose on biological processes affecting water
quality in earthen fish ponds. Environmental Biology of Fishes, 68:247–260,
2003.
[40] R. L. Naylor, R. J. Goldburg, J. H. Primavera, N. Kautsky, M. C. M. Beveridge,
J. Clay, C. Folke, J. Lubchenco, H. Mooney, and M. Troell. Effect of aquaculture
on world fish supplies. Nature, 405:1017–1024, 2000.
[41] R. L. Naylor, R. W. Hardy, D. P. Bureau, A. Chiu, M. Elliott, A. P. Farrell,
I. Forster, D. M. Gatlin, R. J. Goldburg, K. Hua, and P. D. Nichols. Feeding
aquaculture in an era of finite resources. Proceedings of the National Academy
of Sciences of the United States of America, 106:36:15103–15110, 2009.
[42] A. Neori, M. Troell, T. Chopin, C. Yarish, A. Critchley, and A. H. Buschmann.
The need for a balanced ecosystem approach to blue revolution aquaculture.
Environment: Science and policy for sustainable development, 49:3:36–43, 2007.
[43] R. E. Olsen, J. Suontama, E. Langmyhr, H. Mundheim, E. Ringo, W. Melle,
M. K. Malde, and G. I. Hemre. The replacement of fish meal with antarctic
krill, euphausia superba in diets for atlantic salmon, salmo salar. Aquaculture
Nutrition, 12:280–290, 2006.
[44] D. Pauly and V. Christensen. Primary production required to sustain global
fisheries. Nature, 374:255–257, 1995.
[45] K. Powell. Eat your veg. Nature, 426:378–379, 2003.
[46] Barbara J. Rice and Janet Overton, editors. Committee on Animal Nutrition,
Board on Agriculture and National Research Council. Nutrient requirements of
fish. National acadamy press. Washington, D.C., 1993.
[47] Arjen Roem. Interview. Wageningen University, Department of Animal Sci-
ences, Aquaculture and Fisheries. 7-18-2013., 2013.
[48] Craig S. and Helfrich L. A. Understanding fish nutrition, feeds, and feeding.
Virginia Cooperative Extension, 420:256, 2009.
[49] J. Shepherd. Fishmeal and fish oil. sustainability and world market prospects.
International aquafeed, 8:19–21, 2005.
46
51. Bibliography
[50] A. Tacon. Estimated global aquafeed production and aquaculture in 1997 pro-
jected growth. International aquafeed, 2:5, 1999.
[51] A. G. J. Tacon and S. S. DeSilva. Feed preparation and feed management
strategies within semi-intensive fish farming systems in the tropics. Aquaculture,
15:1:379–404, 1997.
[52] A. G. J. Tacon, M. R. Hasan, and M. Metian. Demand and supply of feed
ingredients for farmed fish and crustaceans. trends and prospects. FAO fisheries
and Aquaculture technical paper, Paper No. 564:87, 2011.
[53] A. G. J. Tacon and M. Metian. Global overview on the use of fish meal and fish
oil in industrially compounded aquafeeds. trends and future prospects. Aqua-
culture, 285:146–158, 2008.
[54] A. G. J. Tacon and M. Metian. Fishing for feed or fishing for food: Increasing
global competition for small pelagic forage fish. AMBIO, 38:6:294–302, 2009.
[55] A A. van Dam, M. C.M. Beveridge, M. E. Azim, and M. C.J. Verdegem. The
potential of fish production based on periphyton. Reviews in Fish Biology and
Fisheries, 12:1–31, 2002.
[56] C. D. Webster, D. H. Yancey, and J. H. Tidewell. Eeffect of partially or to-
tally replacing fish meal with soybean meal on growth of blue catfish, ictalurus
furcatus. Aquaculture, 103:141–152, 1992.
[57] Y. Yang, S. Xie, Y. Cui, W. Lei, X. Zhu, Y. Zhu, Y. Yang, and Y. Yu. Effect
of replacement of dietary fish meal by meat and bone meal and poultry by-
product meal on growth and feed utilization of gibel carp, carassius auratus
gibelio. Aquaculture Nutrition, 10:289–294, 2004.
[58] R. D. Zweig. Freshwater aquaculture in management for survival. AMBIO,
14:66–74, 1985.
47
