Review Article

CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2006 1, No.
062
Review
Intensifying aquaculture production through new approaches

to manipulating natural food
M. E. Azim* and D. C. Little
Address: Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland UK.
*Correspondence: Email: meua1@stir.ac.uk
Received:
Accepted:
9 October 2006
30 November 2006
doi: 10.1079/PAVSNNR20061062
The electronic version of this article is the denitive one. It is located here: http://www.cababstractsplus.org/cabreviews
g
CABI Publishing 2006 (Online ISSN 1749-8848)
Abstract
The bulk of the world aquatic production is comprised of herbivorous/omnivorous fish species
that feed low in the food chain and are cultured in semi-intensively managed earthen ponds in the
tropics and sub-tropics. This review summarizes the basic principles and mechanisms of natural
food-based production and explores the potential of novel aquaculture technologies that aim to
further improve nutrient efficiency and overall sustainability. There is a strong linear relationship
between primary productivity and fish yields in earthen ponds. Primary productivity depends
mainly on the availability of elementary nutrients (N, P and C) and sunlight. Fertilization and liming
are common practice in aquaculture ponds to maintain natural productivity and water quality. The
practical upper limit for net primary productivity (NPP) is 4 g C/m2/day but most of the aquaculture ponds remain within the productivities between 1 and 2 g C/m2/day. Pond food organisms
are rich sources of protein and energy, containing 964% and 924 kJ/g, respectively, on a dry
matter weight basis. The nutritional requirement of most pond fish species ranges from 1755%
protein and 1530 mg/kJ protein: energy ratio. Considering an average pond productivity of
2 g C/m2/day, an estimated total fish production of 10 t/ha/yr can be achieved without any supplementary feed, but in practice this is rarely achieved. Polyculture and integrated agriculture
aquaculture (IAA) are traditional in Asia. The reported maximum polyculture production is about
15 t/ha/yr. The term integrated multi-trophic aquaculture (IMTA) has been used in developed
countries as a synonym for polyculture. Aquaculture is integrated with other activities, most
commonly domestic, agricultural or agroindustrial in using resources (water, nutrients and labour)
to improve the use of otherwise underused or sometimes potentially damaging waste materials.
Aquaculture using treated wastewater has also been successful in recent years: production being
reported at 57 t/ha/yr. To enhance pond productivity in the form of periphyton, vertical hard
substrates are introduced in ponds. The reported increase in fish production through the use of
substrates ranged from 30115% in carp monoculture and 30210% in carp polyculture. An annual
maximum production of 9 t/ha was reported from periphyton-based polyculture ponds without
any supplementary feed. The activated suspension technique provides continual aeration and
mixing of the organic matter throughout the water column, thus keeping the decomposition
process aerobic and fast. It is based on the development of dense micro-organisms that function
both as a bioreactor controlling water quality and as a protein food source for the cultured
animals. The technique increases the feed protein utilization and water use efficiency, leading to
reduction in overall costs. We conclude that the novel approaches to manipulating natural food
can increase the productivity and efficiency of aquaculture production systems, and seem to be
conformed to the criteria for ecological aquaculture and organic aquaculture with little modifications based on other specific criteria. More research is needed for optimization of the novel
technologies. Directions for future research are recommended.
Keywords: Natural fish food, Polyculture, Integrated multi-trophic aquaculture (IMTA), Wastewater-fed
aquaculture, Integrated agricultureaquaculture (IAA), Periphyton, Activated suspension technique
http://www.cababstractsplus.org/cabreviews
Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources
Objectives, Scope and Methodology

of the Review
The main objective of this review is to assess the possibility of intensifying aquaculture production through
manipulation of in situ natural food production. We present an overview of the basic principles of aquaculture
production and intensification and quantity and quality
of natural fish foods in aquaculture systems. The means
for increasing natural productivity is discussed and the
potential fish production based on natural productivity is
estimated. We examine the strategies used by fish to
utilize natural food and assess its value in the light of
known nutritional requirement of fish. The role of artificial feed supplementation is also discussed. Finally,
efforts to improve the use of natural food through refined
practices and novel techniques are reviewed. In conclusion, we indicate knowledge gaps for maximizing and
utilizing natural foods and make recommendations for
future research.
The review is based mainly on our own understanding
of different phenomena in pond ecology and aquaculture.
We collected information from the online databases CAB
Abstracts, Science Directory and Synergies. Efforts were
made to collect the full manuscripts from university
library, where these were not available online. We used
our own collection as well. We also spoke to colleagues
who are working in the relevant fields of research
and checked for any relevant findings which are not yet
published.
Overview of Aquaculture Production,

Intensification and Trends
Aquaculture has been practiced as an extensive form
of agriculture by fish and shellfish farmers for thousands
of years in Asia particularly in China. Seaweeds and
freshwater aquatic plants are also widely produced,
often in large quantities. The farmers learned the techniques through trial and error and shared them
among themselves. Scientific or technological advances
in aquaculture only began in the late 19th century
especially in Europe and North America (for review
see 1, 2).
Fish production through aquaculture occurs in a wide
variety of culture systems, depending on location, the
nature of the water environment and culture intensity.
Aquaculture systems may be land or water-based [3].
Land-based systems are located on dry land and include
mainly ponds, raceways and rice fields. These systems
were first developed in China with its relatively small
coastline, a wetland-based agriculture and high densities of
aquatic food eating people providing a strong incentive to
develop land-based aquaculture systems. Water-based
systems are usually situated in inland or sheltered coastal
waters, and include enclosures, cages, pens and rafts.
These systems were first developed in countries with

extensive coastlines (e.g. Japan), where marine fish and
shellfish resources were formerly sufficient to supply their
populations needs [1]. However, the majority of aquaculture production comes from land-based freshwater
culture systems.
Aquaculture systems have been variously characterized
based on the water environment, (freshwater, brackish
water and marine), location (inland, coastal) or by level
of intensity i.e. extensive, semi-intensive and intensive.
Extensive production in any water body is based on
natural productivity and solar energy. Nutrients are not
supplied directly and thus the level of natural food
(plankton, periphyton, detritus and macrophytes) is
limited and tends to support low fish yields. In semiintensive systems, the natural food supply is enhanced
through the use of organic and inorganic fertilizers and/or
low-cost supplementary feed such as rice bran, oil cake
and other agricultural by-products. Earthen ponds in
various forms are the most common unit of extensive and
semi-intensive systems and contribute the bulk of the
worlds aquaculture production. Typically, they also fulfil
other roles at the level of household, community or
watershed, such as irrigation and domestic water supply.
In intensive systems, high stocking densities of fish are
raised on high-quality complete feeds and produce a
greater output per unit production system [4]. This is
usually achieved through higher levels of technology but
necessitates a greater level of investment and incurs
higher risk. However, intensive systems are not always
technically complex and management is species- and
system-specific. Whereas water quality is carefully
maintained through filtration systems in recirculation
aquaculture systems (RAS), cages in rivers may maintain
even higher stocking densities of the same species simply
through their location in a natural river flow.
In 2004, the reported total aquaculture production
(excluding aquatic plants) was 45.5 million tons by weight
and US$ 63.4 billion by value [5]. Production is dominated
by low-income food-deficit countries (LIFDCs), which
account for more than 90% of world aquaculture
production. The contribution of aquaculture to global
supplies of fish, crustaceans and molluscs, continue to
grow, increasing from 3.9% of total production by weight
in 1970 to 30% in recent years, making aquaculture the
fastest growing animal production sector. It is particularly
significant that aquaculture production in LIFDCs has
been growing at a rate exceeding 10% per year since
1970, based mainly on semi-intensive, pond production of
low trophic species (Figure 1). In contrast, aquaculture in
developed economies tends to be intensive, based on
carnivorous species and has maintained less than half
this level of growth (Figure 1). Sustaining such growth has
proved controversial, however [6, 7], and there are
concerns that LIFDCs will need to move towards a more
industrial approach to fish farming, based on fishmeal- and
fish oil-based formulated diets.
M. E. Azim and D. C. Little
Figure 1 Relative nsh production and degree of

intensication in LIFDCs and industrialized countries
Complete formulated diet
Contribution of formulated diet (%)
Global production (million tons)
Natural supplemental food
Figure 2 Global meat and aquaculture production and

their dependence on formulated diets
Feed-driven systems, however, are inefficient if feed

nutrient conversion efficiency around 20% [8] is considered. Further, the proportion of nutrients that can
be reused is highly system- and context-specific, the
remainder being lost to the environment. A total of 43%
of global beef and more than 50% of global pork and
poultry production are based on formulated diet, whereas
less than 10% of global aquaculture is based on complete
formulated diet (Figure 2). In addition, all livestock,
including fish fed formulated diets, indirectly consume
large quantities of water. On average, 1200 litre of water
is needed to produce 1 kg of grain used in animal feeds. To
gain 1 kg weight, cattle, pigs and poultry consume about
7, 4 and 2 kg of feed concentrates, respectively. In contrast, fish or crustaceans require less than 2 kg of grain
concentrate for each kg produced, making them the most
efficient producing animals in terms of feed-associated
water use [9]. However, more intensive aquaculture
is more efficient in its direct use of water than semiintensive [9]. Any holistic assessment of water use efficiency requires that impacts of any change in water quality
that occurs after use to be considered.
Improving the resource efficiency of aquaculture

systems needs to recognize both economic and environmental realities. A central issue is the resource efficiency
of the culture system itself and, secondly, the impact of
the production unit viewed within a broader system. To
this end, aquaculture can evolve in two directions: (1)
specialization and intensification of inland monoculture
production, involving sophisticated technologies for
feeding, water quality management and waste treatment,
and (2) integration of less intensive aquaculture within
broader agricultural systems. Both routes can potentially
be sustainable and environmentally sound but the latter
currently fits more easily into the emerging concepts
of ecological aquaculture and organic aquaculture [10].
Aquaculture has an opportunity to move away from
optimizing production per se towards integrated management of natural resources and ecosystems [11] and to
incorporate comprehensive planning for the wider social,
economic and environmental contexts [12].
Relatively little research effort has been devoted to
improving the production and utilization of in situ natural
fish food despite its importance. This contrasts to the
focus on intensification of aquaculture. New approaches
to sustainable aquaculture production that meet the
needs of both producers and consumers are urgently
required. Maximizing and utilizing natural foods in production systems might be such an option. To this end,
traditionally practiced polyculture and integrated aquaculture need to be improved and some novel concepts,
namely periphyton-based aquaculture, activated suspension techniques (AST), integrated multi-trophic aquaculture (IMTA), etc. need to be tested for their potential
application.
Ecology of Pond Aquaculture

In aquaculture ponds, complex interrelated physical,
chemical and biological processes contribute to the formation and the stability of the ecosystem. For simplicity,
three basic ecological processes can be distinguished:
production, consumption and decomposition (Figure 3).
Production is based on the conversion of solar energy,
carbon dioxide and dissolved inorganic nutrients into
plant biomass and oxygen through photosynthesis. It leads
to the formation of phytoplankton, periphyton and other
submerged plants, providing the base of aquatic food
webs. This base can be supplemented by the addition of
organic matter in the form of manure or artificial feed.
In the consumption process, both autochthonous and
added organic matters are eaten directly or indirectly by
aquatic animals such as zooplankton, benthos, fish or
shrimp providing energy and building blocks for biomass.
Decomposition is the third basic ecological process consisting of the breakdown and mineralization by microorganisms (bacteria, protozoa and fungi) of organic matter
leading to the formation of detritus and inorganic
Production
Consumption
(Plants)
(Animals)
Nutrients
exchange
(Biotic and abiotic factors)
Decomposition
(Bacteria)
Figure 3
pond
Aquacultural ecology: nutrient exchange through production, consumption and decomposition processes in a sh
nutrients. The detritus is consumed directly by the cultured fish or crustaceans or by other small animals on
which the cultured species feed [13, 14]. The inorganic
nutrients released as a consequence of this consumption
are then available for reuse after uptake through the
autotrophic food web (Figure 3).
The direct use of primary production (phytoplankton)
by fish depends largely on the trophic level of the fish
species stocked and their specialized feeding strategy.
Carnivorous species are clearly inefficient but many
omnivorous and herbivorous species are also unable to
utilize directly the nanoplankton that dominate warm
water ponds [15]. Estimated energy transfer efficiencies of
10% per trophic level [16] result in theoretical maximum
fish yields being no more than 1% of the energy fixed by
autotrophs per trophic level. Therefore, fish yields from
extensive and semi-intensive ponds could be up to ten
times higher if primary production could be harvested
directly by herbivorous fish. Fish species that feed lower
in the food chain, i.e., herbivorous and omnivorous
fish are, therefore, the most efficient to culture in
phytoplankton-dominant systems, although such species
do not always realize the highest market prices.
Natural Fish Food: Quantity and Quality

The common natural foods for fish in an aquatic system
are autotrophs, heterotrophs and detritus. Autotrophic
food is comprised of phytoplankton (algae), periphyton
(attached algae) and aquatic macrophytes. However,
aquatic macrophytes are less important in fertilized ponds
and kept control since they compete with algae for
nutrients. Heterotrophic food includes bacteria, protozoans, fungi, zooplankton and benthos (micro- and macroinvertebrates). Detritus is composed of non-living organic
particles originating mainly from dead parts of both
autotrophic and heterotrophic organisms. Three key

points are very important in natural food based aquaculture: (1) the amount of natural food available for fish
and the regeneration capacity of these food organisms
under grazing pressure, (2) nutritional quality/composition
of these food, and (3) the ability of the fish species to
harvest, select, digest and assimilate of these food.
Whether a fish species selects a specific food is dependent
not only on the inherent preferences of the fish for
its food, but also on the overall abundance of food,
the quantitative relationships between the food items,
the accessibility of these food items, and the degree of
satiation of the fish [17].
There are two basic food sources for all organisms in
extensive and semi-intensive ponds: (1) primary productivity from algae, and (2) added organic matter as
feed or manures (also discussed in the previous section).
Secondary trophic level feeders (zooplankton, benthos,
invertebrates, etc.) including fish utilize the organic matter
produced by algae through photosynthesis. In the latter
case, organic matter applied as supplementary feed or
manures enhances primary productivity and fish production through direct or indirect consumption by fish. In
both cases, heterotrophic micro-organisms (bacteria,
protozoa and fungi) are essential components of the food
web because these organisms decompose organic matter
and release nutrients, which can again be utilized by algae
or consumed by the fish [13, 14]. Sometimes, inorganic
fertilizers are also added to increase autotrophic production. However, nutrient inputs to optimize natural
food availability and quality need to be balanced
with maintaining water quality parameters suitable for
respiration and other functions of the fish in any aquatic
system.
In general, there is a strong positive linear relationship
between primary productivity and fish yields in ponds
[13, 18, 19]. The primary productivity of a pond depends
Table 1 Reported net primary productivity (NPP) of sh ponds

Location
Management
NPP (g C/m2/day)
References
Thailand
Indonesia
Honduras
Panama
India
Bangladesh
Phosphorous fertilization
Inorganic and organic fertilization
Chicken litter
Inorganic and organic fertilization with
periphyton substrates
1.6
0.81.9
0.32.4
1.74.4
0.71.4
2.23.0
[18]
[18]
[18]
[18]
[19]
[20]
Table 2 Proximate composition of natural sh foods in earthen ponds (Values are expressed in % dry matter basis)
Group
Ash
Crude
protein
Crude
lipid
Carbohydrate
Energy
(kJ/g)
References
Phytoplankton
Plankton (mixed)
Microalgae (cultured)
Periphyton
1
Detritus
Rotifers
Cladocerans
Copepods
Artemia
Oligochaetes
Molluscs
Chironomids
2747
825
514
1447
6
8
7
10
6
33
6
1831
2750
1340
932
015
64
57
5258
3062
49
40
59
410
25
1027
0.56
20
19
714
1828
19
8
5
549
3352
28
8
23
916
1823
1220
415
20
20
23
24
23
16
21
[22]
[23]
[24]
[25]
[26]
[27]
[27]
[27]
[27, 28]
[22]
[22]
[22]
ash free dry matter basis (AFDM).
mainly on the available inorganic nutrients and sunlight.

Therefore, primary productivity is linked to the pond
surface area rather pond depth and varies significantly in
different geographical locations. The practical upper limit
for net primary productivity (NPP) is 4 g C/m2/day but
most aquaculture ponds remain within the range 12 g C/
m2/day (Table 1). Since the primary productivity is lightdependent, there is the limit of production and therefore,
fish stocking density must be adjusted to the amount
of available natural food in semi-intensive ponds. Unfortunately, our knowledge regarding the relationships
between levels of natural food, fish density, individual
growth rate and yield is very limited. Although individual
growth rate can be changed by environmental manipulation and selective breeding to some extent [21], the
growth rate is principally physiologically limited. Therefore, the principal way to increase yield per unit area is
through increasing the density. As long as the amount of
natural food exceeds requirements for maintenance and
maximum growth, an increase in fish density should not
affect the individual growth rate of the fish [22], provided
that adequate water quality is maintained.
The biomass of fish food organisms in a pond, the
proportion of each food species, and their chemical
composition vary constantly due to changes in environmental conditions and the effects of selective grazing and
predation by fish. The nutritional quality of natural food
organisms in ponds varies over a large range (Table 2).
In general, animals have higher nutritive quality than
plants and detritus has highly variable, but significantly

lower, levels of crude protein and metabolizable energy.
Generally, food organisms found in ponds are a rich
source of protein and energy, containing 964% and
924 kJ/g, respectively, on a dry matter (DM) basis. The
availability and digestibility of the major food organisms
are discussed later.
Increasing Productivity in Aquaculture Ponds

Fertilization, liming and in some cases, mechanical aeration are used to enhance natural levels of productivity.
Fertilization in ponds can be based on organic or inorganic
forms and nitrogen, phosphorous and occasionally carbon
are the most common limiting nutrients. Pond fertilization
is traditional and practiced extensively, but a more
scientific approach is relatively recent. Compared to
terrestrial pasture research, for example, where the
principles were established in producing specific grass
cultivars [29], little is known about the specific nutritional
requirements of desired phytoplankton species or how to
manage less desirable or undesirable species within the
pond food web.
Under optimal growth conditions, the average nutrient
composition of phytoplankton is in the range 4550% C,
810% N and 1% P, giving a typical C : N : P ratio of about
50 : 10 : 1 [30]. In a recent review, Kumar et al. [31]
reported that the 1 ppm N : 0.5 ppm P (ratio 2 : 1)
concentration was found to be the most suitable nutrient

ratio for pond fertilization resulting in higher fish production. They recommended regional research to optimize fertilization focusing on significant climate variability,
which affects both primary and secondary production.
However, the required quantity of fertilizer varies significantly with time since the pond management history
including previous fertilization has a residual effect [32].
Knud-Hansen et al. [33] compared three fertilization
strategies to determine fertilization rates for producing
natural foods in semi-intensive aquaculture ponds: (1) a
predetermined, fixed-input rate of N and P based on
results from previous yield trials, (2) a microcomputerbased expert system in combination with biweekly water
quality measurements, and (3) algal bioassay fertilization
strategy (ABFS) based on algal growth response to
nutrient enrichment and pond-specific algal bio-assays to
determine both nutrient requirements and associated
rates of required nutrient inputs. Based on this study, the
recommended fertilization strategy designed to achieve
cost-efficient, consistently high yields is a modified ABFS
approach that uses a fixed-input fertilization rate for N
(30 kg/ha/week), and algal bioassays to determine timespecific and pond-specific fertilization requirements for
P and C. The frequency of pond fertilization was investigated with mixed results: Garg and Bhatnagar [19]
reported that the highest values of fish biomass, specific
growth rate (SGR), NPP, plankton population and nutrients were observed in the ponds that were fertilized
twice a month, whereas Wahab et al. [34] suggested
weekly fertilization for sustained pond productivity.
The common fertilizers used in aquaculture ponds
include a range of animal manures (livestock, poultry
and human manures) and commercial fertilizers (urea,
ammonium nitrate/sulphate, mono/triple superphosphate,
diammonium phosphate, etc.). In recent decades, there is
a growing interest of using biofertilizer in aquaculture
ponds. Inoculation of Azobacter enhanced NPP and
fish biomass in still water ponds [35]. Azolla showed a
similar performance in carp culture ponds [36]. The best
performance was evident in ponds provided with biofertilizers in combination with other fertilizers in both
studies. However, because of the growing concern about
conservation of the environment and the need for
deploying renewable, sustainable resources, the application of biofertilizer in aquaculture ponds, in order to
provide a natural source of the crucial nutrient nitrogen,
can be very beneficial to the future aquaculture practices.
Many aquaculture farmers especially in Asia cannot afford
chemical fertilizers to their ponds. Biofertilizer application
can enhance their economic status, increasing yields while
minimizing costs. The use of biofertilizer also meets the
criteria of organic aquaculture.
The pH of pond water mainly depends on the bottom
soil pH. Pond liming is commonly practiced in areas with
acid soils and soft waters but is not necessary in areas
where water supplies or soils have high concentrations of
carbonates. The immediate goal of liming is to neutralize

soil acidity, i.e. to decrease base unsaturation to nearly 0%
and increase soil pH to the near neutral range. Benefits
that may result from applications of lime to the pond
bottom include: (i) increases in the availability of nutrients
from the bottom soil [37], (ii) increased benthic production [38], (iii) increased microbial activity in the mud [39],
and (iv) increased fish production [40]. In general, pH
value less than 6.0 for pond soils and total alkalinity
value less than 20 mg/l in pond waters are the indicators
of lime requirements for ponds [41]. Lin et al. [18]
have suggested use of lime to maintain alkalinities above
5075 mg CaCO3/l, when fertilizing at maximum rates.
Dissolved oxygen is one of the most limiting factors in
pond aquaculture and produced as a byproduct of phytoplankton photosynthesis. The oxygen requirement in
ponds depends mainly on the biomass and productivity of
phytoplankton, fish species cultured, stocking density and
feeding level [42]. In semi-intensive ponds stocked with
relatively high stocking density, mechanical oxygen supply
is required especially at late night until the photosynthesis
starts after sunrise. Circulation of pond water throughout
the day can increase overall dissolved oxygen levels. This
can eliminate the stratification that develops between the
bottom oxygen-poor water and the top layer of oxygenated water. Simple mechanical aeration and air bubble
devices are a low energy and effective means of increasing
oxygen availability in ponds [43]. Boyd and Tucker [42]
reviewed the effects of pond aeration and concluded
that the pond aeration increased fish production, feed
conversion efficiency and profitability. In a recent study,
Qayyum et al. [44] reported that pond aeration resulted
in 5000 kg/ha more fish production in a four species
polyculture system in Pakistan. However, the benefit to
natural food production through physical aeration and
water circulation, resuspending nutrients and aggregated
detritus, may also be important, and supplement that from
the movement and activity of the fish themselves [43].
Herbivorous and Omnivorous Fish Species and

their Nutritional Requirements
Not all fish can utilize autotrophic food resources which
are the main components in an aquaculture pond. In
principle, fish species that feed low in the aquatic food
chain are suitable for pond aquaculture based on endogenous/natural food. However, many of the herbivorous
fish species are opportunistic omnivores and eat animal
components in suspended, attached and benthic assemblages. The commonly cultured herbivorous and omnivorous fish species in aquaculture include the Indian major
carps, Chinese carps, tilapias, milkfish, mullet and various
species of gourami and barbs. Most of these species have
some particular physical and behavioural adaptations
for searching, selecting and processing plant materials.
Searching food is guided by external taste buds packed on
Table 3 Adaptations to herbivory

Adaptations
Functions
External taste buds on

barbells or lips
Specialized gill
rakers/jaw teeth/mucus
Pharyngeal/muscular
intestinal mill
Long intestine
To search and select food
Low stomach pH
To capture food
To grind vegetation and
rupture cell walls
To increase the residence
time of food
To enhance ingestion and
digestion
barbels (e.g. cyprinids) or on the lips and buccal cavity

(cichlids). Food is captured by suction, biting, grazing or
mucus entrapment depending on the special food cropping equipments (size and shape of the mouth, gill rakers
and filaments, jaw teeth, mucus, etc.) that fish possess.
The entrapped material is transferred to the buccopharyngial cavity. Once in the buccal cavity, food material
is sorted and either rejected or accepted. The accepted
material is then masticated and raked towards the oesophagus and swallowed [45]. Specialization towards a plant
diet processing requires adaptation of the teeth (from
grasping to cropping teeth), a grinding apparatus, a less
acidic stomach and a longer gut length (Table 3; for
details, see Sibbing and Witte [46]). Pharyngeal and
muscular intestinal plates grind vegetation to rupture cell
walls, low pH stomach interferes with the ingestion and
digestion and a longer gut length is to increase the residence time of food, thus enhancing digestion [47, 48]. Fish
generally possess the enzymes to digest the contents of
plant cells, but lack the enzymes capable of disrupting
cell walls by digesting the beta-linked polymers, such as
cellulose [49]. Cellulase activity in fish guts can probably
be ascribed to micro-organisms colonizing the fish gut
contents [50].
The quantitative requirement for any specific food item
by fish depends largely on the composition of food. The
correct supply of energy and essential nutrients in the
proportions through food required by the fish is essential
for proper maintenance and growth of the fish. Unfortunately, there is hardly any reliable information on
nutritional requirements of herbivorous and omnivorous
fish species (with exception of few species of tilapias and
common carp): most research has concentrated on carnivorous fish and shellfish species. Some available information on dietary requirement of some pond fish species
is presented in Table 4. The requirements are highly
variable even within the same species and related to size,
age and culture system. Such estimations are based on the
artificial feeds from which extrapolation to natural food
organisms are unreliable. Crude protein requirements
ranged from 17 to 55% and protein: energy ratio
ranged from 15 to 30 mg/kJ on a DM basis. According to
Hepher [22], the nutritional requirements of most of the
semi-intensively cultured organisms range from 2835%

protein and 23 mg/kJ protein to energy ratio.
Potential Fish Production Based on Natural

Productivity
There are hardly any quantitative data on the digestibility
and utilization of natural foods by fish and therefore
it is difficult to estimate the potential fish production
exclusively based on natural pond productivity. However,
a simulation model has been developed by Li and
Yakupitiyage [66] incorporating elementary nutrients (N
and P), food nutrients (both autotrophs and heterotrophs
and/or supplementary feed), dissolved oxygen and fish
growth. The model was run for a Nile tilapia monoculture
(4000/ha) in fertilized earthen ponds fed an energy-rich
supplement. The simulation, the results of which of the
model fitted well with the experimental data, predicted an
extrapolated net production of 10 155 kg/ha/yr. However,
this production was not completely based on natural
productivity since applied carbon sources could have a
direct effect on heterotrophic food production as well as
fish growth to some extent.
The limits to natural food based fish production can
also be estimated from the NPP of ponds. Considering an
average pond productivity of 2 g C/m2/day (from Table 1),
an estimated annual C production would be 7300 kg/ha,
equivalent to 18 250 kg/ha phytoplankton dry matter
(assuming 40% C content in phytoplankton DM; [67]).
Again, considering the average protein content of phytoplankton is 30% DM (Table 2), an estimated 5475 kg DM
crude protein can be produced annually in one hectare
pond. Azim et al. [68] reported a protein conversion ratio
(dry protein fed/fresh weight gain) of 0.5 in a laboratory
study feeding tilapia with fresh periphytic algae. Using this
FCR value for phytoplankton, an estimated fish production of 10 950 kg/ha/yr can be achieved based on primary
productivity alone. However, these calculations ignore the
complexity of pond food webs; this level of production is
not realized in fertilized ponds without supplementary
feeding. Indeed, Azim et al. [69] reported a maximum net
extrapolated yield of 9000 kg/ha/yr from pond studies in
Bangladesh provided with fertilizers and periphyton substrates without applying any supplementary feed. Tilapia
utilizes natural food organisms so efficiently that standing
crops of fish exceeded 8500 kg/ha/yr in well-fertilized
unfed ponds in Honduras [70] and Thailand [71]. Elsewhere, yields were lower and/or more erratic, reflecting
differences in climate, management and species combination. Sarig [72] reported a fish production of up to
3000 kg/ha annually in fertilized ponds. Fish production in
the treated waste effluent, without supplementary feeding
or pond aeration, reached 50007000 kg/ha/yr in Egypt
[73]. However, many factors reduce practical yields from
the potential optimum, including dominance of food webs
by undesirable phytoplankton species, oxygen depletion
Table 4 Nutritional requirements of some pond sh. Values are given in dry matter weight basis
Fish species
Crude
protein (%)
Crude
lipid (%)
CHO
(%)
P : E ratio
(mg/kJ)
Chanos chanos
Mugil capito
Ctenopharyngodon idella
Cyprinus carpio
Labeo rohita
Catla catla
Oreochromis aureus
Oreochromis niloticus
Hybrid tilapia (O. niloticusO. aureus)
Tilapia zillii
Oreochromis mossambicus
Ictalurus punctatus
Siganus spp.
Pangasius sutchi
3040
28
2328
3046
2536
38
3640
2845
2835
3540
2955
2440
1740
2729
10
78
78
10
15
12
15
510
2545
3040
2230
2230
2530
3738
26
1530
1922
2629
2629
27
2325
2428
2023
1525
19
References
[5154]
[55]
[55]
[22, 5557]
[5862]
[62]
[63]
[63]
[63]
[63]
[63]
[64]
[54]
[65]
Requirement of
supplementary feed
Figure 4 The relationship between natural food biomass and sh yield in relation to the standing crop of stocked sh and
requirements of supplementary feed (modied from De Silva and Anderson [75] with permission from Chapman and Hall)
and difficulties in maintaining steady productivity due to

fluctuation of sunlight and temperature, etc.
Requirement for Feed Supplementation

The major rationale for use of supplementary feeding
within fertilized systems is that stocking density and yield
can be increased to more profitable levels. Supplementary
feeds, by definition, supplement a natural feed base that is
high in crude protein and micronutrients and therefore,
tend to be energy rich. The energy-rich, relatively low
cost nature of supplementary feeds means that they are
ineffective if used in systems deficient in natural food and
hence fertilization strategies are critical. The use of supplementary feeding needs to be related to the management of the pond as a system. Maximum growth is a
common goal for any aquaculture system and ponds are

typically stocked with a low biomass of young fish that
grows at, or near, maximum rate until natural food or
other environmental conditions become limiting. This
point is termed as the critical standing crop (CSC), which
is the biomass of fish in any aquaculture system that
results in a reduction of individual growth. Even though
individual growth rate is reduced at CSC, biomass continues to increase once the CSC is exceeded until the
population reaches carrying capacity. At carrying capacity,
density effects of the population are so strong that individual growth reaches zero, and biomass remains
stable [74]. With an increase in standing crop and a
resultant limitation in natural feed deficit, the relative
amount of supplementary feed required to support
growth increases (Figure 4). As the relative amount of
natural feed declines and CSC is exceeded, there is also a
need to increase the crude protein and micronutrient

quality of any supplementary feed given. Alternatively,
fish density can be reduced or a lower growth rate
accepted [75].
Supplementary feeding has to be considered as part of
overall dry matter and nutrient loading to the pond to
ensure that water quality can be maintained at levels
tolerable for growing fish. Now, the question is how much
supplementary feed can be added in a semi-intensive pond
without deterioration of water quality occurring given
that 80% feed nutrients are lost to the environment. This
can be estimated by the carbon fixation rate through
photosynthesis and its ammonia uptake capacity resulted
from the artificial feed using Redfield stoichiometric
ratios (atomic C : N : P=106 : 16 : 1). Semi-intensive ponds
fix between 1 and 4 g C/m2/day (Table 1), equivalent to
ammonia uptake of 150600 mg N/m2/day. If the supplementary feed contains 30% crude protein, then feeding
within a range of 37.5150 kg/ha/day can be applied to
the semi-intensive fertilized ponds without any ammonia
problems. Greater feeding rates are still possible but
they need additional assimilative mechanisms like nitrification and heterotrophic immobilization to remove the
additional ammonia. However, phytoplankton uptake of
ammonia is a temporary and partial packaging of nitrogen
in the form of cellular protein, eventually as much as
50% of the algal standing crop dies off and settles on
the bottom surface [76]. The organic nitrogen contained
in the dead cells are partially utilized by fish and/or
mineralized by heterotrophic bacteria and recycled to the
water as ammonia again.
Manipulating Production Systems

to Enhance Yields
The dependence of a high proportion of global farmed fish
production on natural food management in ponds has
been presented. The relationship between fertilization
strategies to enhance natural feed levels and use of supplementary feeding has been explained. In this section, we
discuss the principles of different approaches to enhancing
natural food production and utilization within aquaculture
systems. These consider both the level of the autochthonous production system itself and surrounding
agricultural and human systems. We also discuss some
new approaches to extensification of more intensive
systems by integrating natural foods for water quality
improvements and/or for consumption by fish.
Polyculture
Polyculture in aquaculture has been reviewed recently by
Milstein [10]. As discussed earlier, aquaculture ponds are
complex three-dimensional (3D) environments containing
several spatial niches and therefore the natural food webs
Figure 5 Chinese polyculture pond. Natural food resources are utilized by the major sh species: grass carp,
Ctenopharyngodon idella (A) and wuchang sh, Megalobrama amblycephala (B) graze on land grasses and
aquatic macrophytes; silver carp, Hypophthalmichthys
molitrix (C) feeds upon phytoplankton; bighead carp,
Aristichthys nobilis (D) consumes zooplankton; tilapia,
Oreochromis sp. (E) feeds on plankton, green fodders and
benthic organic matter; black carp, Mylopharyngodon
piceus (F) eats molluscs; and common carp, Cyprinus
carpio (G) and mud carp, Cirrhinus molitorella (H) consume
benthic invertebrates and bottom detritus (modied
from Zweig [81] with permission from the Royal Swedish
Academy of Sciences)
in pond systems are very diverse. The different spatial

niches and diverse natural food webs can be utilized by
using species with diverse and complementary feeding
habits and niches. In aquaculture, polyculture can be
defined as a management system in which two or more
species of complementary feeding habits and niches, or
different size classes of the same species, are stocked
together in the same production system in order to
maximize available food and water resources, thereby
obtaining high fish production per unit area of a water
body [7779]. In polyculture, synergies also arise from
two interrelated processes: the increase in available food
resources and improvements in environmental conditions
[10, 80]. Normally, ponds are fertilized to enhance natural
fish food organisms in polyculture system. The basic
principle is to occupy all of the ecological niches of a
water body by stocking fish species of different food and
feeding habits and niches so that natural foods of different
strata and zones are utilized properly with minimum
competition and dietary overlaps among co-inhabiting
species or size classes. The balance between complementarity and competition is the essential feature of
polyculture. Appropriate stocking densities and ratios of
cultured animals are therefore required if production is to
be optimized. Figure 5 shows a Chinese polyculture model
indicating different fish species feeding on different niches
in an earthen pond.
There is a great variation in polyculture production,
depending on stocking combination and density of different species, supplementary feed, fertilization and a range
of environmental factors. So far, recorded fish polyculture
production levels around the globe ranged from 1000 to
15 500 kg/ha/yr [72, 8285]. The highest fish production in
polyculture ponds has been reported by Tripathi et al.
10
[82] based on experiments carried out over a duration

of one year with carps stocked at a density of
25 000 fingerlings/ha. Management practices included
application of Azolla as a biofertilizer, provision of aeration
for 46 h during late night hours, balanced supplementary
feed and fish health management.
Although feeding niches of some polyculture species
are reasonably well known, predicting synergisms or
antagonisms between species remains difficult. Availability
of 610 species at stocking is not always easy for farmers
and interspecific competition among many species makes
the technology more complex. Development of 34
species polyculture technique is an alternative option.
Pond polyculture models incorporating both natural food
and supplementary feed could help in understanding the
complex ecology of polyculture production systems.
Increasing intensification of aquaculture systems and
consequent issues over pollution caused by the high
flows of nutrients have prompted interest in polyculture
from a different perspective: nutrient reuse in a context
of overabundance. Recently, the term integrated multitrophic aquaculture (IMTA) has been used in developed
countries as a synonym for polyculture. This system
aims to combine, in optimal proportions, the cultivation
of fed aquaculture species (e.g. finfish) with organic
extractive aquaculture species (e.g. shellfish) and inorganic
extractive aquaculture species (e.g. seaweed), for a
balanced ecosystem management approach that takes
into consideration site specificity, operational limits, and
food safety guidelines and regulations [86]. The aim is
to increase long-term sustainability and profitability of
culture system as a whole, rather than a single species in
isolation, as is the norm for monoculture, as the wastes of
one component (finfish) are captured and converted into
fertilizer, food and energy for the other components
(shellfish and seaweed), which in turn can be sold in the
market as other marine crops [87].
Integrated AgricultureAquaculture (IAA) Systems

An extension of the polyculture concept is the consideration of aquatic system in a broader nutrient and
other resource framework. Most tropical smallholder
pond production is constrained by nutrient limitations and
therefore aquaculture can be integrated within other
farming system [88] in which crop and animal wastes or
by-products are recycled within fishponds to enhance
productivity, and water and mineralized nutrients returned to terrestrial components. Water use, nutrient
transfers, and labour and management inputs can be
synergistic if aquaculture is combined with other activities.
These include domestic, agricultural or agro-industrial, to
improve the use of otherwise underused or sometimes
potentially damaging waste materials [21, 89]. Integration
is used to improve nutrient cycling and overall ecological
efficiency in delivering harvestable and/or marketable
products and, most crucially, in many contexts to widen

employment, income and livelihood opportunities among
poorer households [43, 88]. However, integrated farming
is most associated with increasing nutrient utilization
rather than intensifying aquaculture in different subsystems. Nevertheless, considering the present contribution and future prospects of integrated farming especially
in major aquaculture producing countries, common forms
of IAA systems are discussed briefly in this section.
A complex model of resource flows in integrated
farming systems is depicted in figure 6. Although the
complex nutrient/resource dynamics are not quantified so
far, integrated farming systems are traditionally practiced
in small farm households and have been actively promoted
in many developing countries. Among others, integration
between livestock and fish components is common and
valued. Several studies of small holder aquaculture in Asia
indicate that livestock manures are the most commonly
used pond inputs and support the production of most
cultured fish although the production might not be
optimized for a variety of reasons. However, the most
productive forms of integration between livestock and
fish demand well-designed, co-location of feedlot monogastrics and culture ponds [88]. Livestock, including
poultry-fish integration is most common among resourcerich farmers as the livestock enterprise is dependent on
off-farm formulated feed. High-input aquaculture systems,
often based on high-value carnivorous species, have also
been integrated with semi-intensive systems to improve
financial returns and reduce nutrient effluents. Lin and Yi
[91] investigated the potential of reuse pond effluents and
bottom mud, based on a series of pond experiments of
the most commonly cultured species in Thailand, hybrid
catfish (Clarias macrocephalusClarias gariepinus) and Nile
tilapia (Oreochromis niloticus) in cage-cum-pond systems.
They demonstrated that the major nutrient input from
formulated feed could be effectively recycled in a closed
pond where hybrid catfish were cultured with intensively
fed formulated diets in cages and Nile tilapia with natural
food in an open pond.
Other forms of IAA that are more appropriate for
resource-poor farmers include integration with rice
or other crop production and based on a shared use of
water and/or space as much as improving efficiency of
nutrient use per se. Traditional ponddike systems
in southern China were based on intensive nutrient
recycling over the ponddike interface, resulting in the
retention of 5070% nutrients used in the combined
crops of aquatic and terrestrial component [92]. More
commonly, however, especially where opportunity costs
of labour are high, nutrient linkages between pond
and associated cropping are weak and limited to the
relatively minor amounts of nutrients removed for irrigation of crops produced on ponddikes [93] (Figures 7
and 8). Removal of nutrients trapped in fishpond
sediments can occur in situ if aquatic macrophytes are
produced. Economically valuable rooted aquatic plants,
11
Figure 6 Resource ows among the different farming subsystems on smallholdings in Africa (drawn by Nobel R. P.;
reproduced from Brummett [90] with permission from the WorldFish Center)
such as lotus (Nelumbo mucifera), can remove significant

quantities of nutrients from pond mud (300 kg N and
43 kg P/ha/yr[91]). Effluents from intensively cultured
hybrid catfish culture have also been found useful to
fertilize irrigated rice; 32% total nitrogen (TN) and 24%
total phosphorus (TP) were removed from effluents, and
rice yields were comparable to that based on regular
fertilization [91]. More commonly, rice and fish production has occurred in the same system at the same time
(Figure 9). Expensive inorganic fertilizers are preferentially
used by smallholders in their rice fields than for improving
productivity of fishponds in many areas where rural
aquaculture has been promoted in Asia. In this context,
the management of fish with rice concurrently has been
shown to improve overall system nutrient efficiency [94].
This has been related to the behaviour of fish removing
weeds and disturbing sediments. Rotational rice-fish
culture, in which fish are cultured in re-flooded fields after
rice harvest, can also improve overall nutrient efficiency
and can also result in improved nutrient reuse and
decomposition.
Nevertheless, understanding nutrient efficiency in

aquaculture subsystems is complex, leading Michielsens
et al. [95], based on a survey of 2500 carp farms in
nine Asian countries, to conclude that on average
the aquaculture components of IAA systems are less
nutrient-, land- and labour-efficient than specialized semiintensive fish farms. They found that when aquaculture
was adopted in a semi-extensive mode within other
farming systems, fish yields from ponds were often low
(< 1000 kg/ha/yr).These observations support previous
findings that rural smallholdings rarely feature strong
linkages with respect to nutrient flows between aquaculture and elsewhere in the farming system [88]. Such
smallholdings are highly nutrient deficient and such
nutrients as available are dispersed (through livestock
grazing etc.) and thus less available, more laborious to use,
and frequently of poorer quality. Moreover, purchased
nutrients are typically prioritised for use elsewhere
in the farming system. In contrast, integrated semiintensive systems, presumably based on feedlot livestock
have nutrient efficiencies comparable with specialised
12
Figure 7 Ponddike integration in Sisaket Province, Thailand. Vegetables are grown on dikes and fences hung on the
shpond and pond water is used for them (Photo by M. E. Azim)
enterprises purchasing nutrients from off-farm. The analysis and conclusion point to the dangers of comparing
very different systems under a category IAA with respect
to assessing nutrient or other efficiencies. The poor
outcomes of smallholder IAA have also been related to
the lack of fry or fingerlings and pond inputs, and
importance of other components of integration [96]. A
key to the successful operation of integrated farming
systems is the orchestration of the multi-enterprise
production calendar in such a coordinated manner that
residues from one enterprise are available at the right
time and in the right amounts needed as inputs to other
enterprises [97] but such farming households typically
have to balance such management within a broader
livelihood portfolio [88]. Fish yield alone is too narrow a
criterion to measure the success of IAA systems development. A major issue is that rural farms are resourceand, specifically, nutrient-poor, which limits opportunities
for recycling and raises the issue of whether aquaculture
should be the focus of re-using limited by-products rather
than elsewhere in the farming system. In contrast, urban
and peri-urban areas are often nutrient rich which may
have been a major factor in long established aquaculture
having urban origins [98]. Fish farming based on opportunistic use of wastewater is relatively common in
parts of south and Southeast Asia (discussed in the next
section).
Wastewater-Fed Aquaculture
Informal use of excreta and wastewater in aquaculture is
relatively widespread in parts of Asia, but little practiced
in other parts of the world. In most developing countries,
two-thirds of urban wastewater receives no treatment at
all. The wider use of wastewater for aquaculture has been
proposed, especially as a sanitation option in fast-growing
urban areas of LIFDCs where conventional treatment is
not an option, but there are significant constraints [99].
Rapid attenuation of microbial pathogens typically occurs
in shallow fish ponds and most holistic risk assessments
[100] support the integration of aquaculture as a valuable
component of low-cost sanitation. There is also growing
interest in use of treated effluents in many parts of the
world because of a critical shortage of renewable water
resources, especially in semi-arid and arid regions.
Normally, the nutrients contained in wastewater are used
to produce natural food such as plankton and benthos
for fish or taken up by aquatic plants directly. Most
wastewater is used directly to produce herbivorous and
omnivorous fish, mainly Chinese and Indian carps, catfish
and tilapias, or aquatic plants such as lotus, water mimosa
and water spinach for human food. There is also production of fish seed or fingerlings and aquatic plants
especially duckweed, to feed livestock and herbivorous
fish [99].
13
Figure 8 Ponddike integration in Mymensingh district, Bangladesh. Pond water is used for production of fruits and
vegetable on the dikes (Photo by M. E. Azim)
The use of waste stabilization pond effluent within IAA

has been successful in several different contexts. For
example, yields of two local fish species, O. niloticus and
Mugil sehli reached 50007000 kg/ha/yr without supplementary feeding or aeration in Egypt [73]. The
nutrient-rich effluent from the fishpond was further used
to grow trees and cultivate certain types of crops,
i.e. barley, maize, beets and ornamental plants. Hoan
and Edwards [101] reported nearly 7000 kg/ha fish
production in wastewater-fed fishponds in Vietnam during
a 10-month culture period. A wastewater-fed aquaculture
pond in peri-urban Hanoi is shown in figure 10. Major
constraints include the contamination of domestic with
industrial wastewater that makes exclusion of potentially
toxic products from the food chain a challenge. The
potential risks of bio-accumulation of health-hazardous
chemicals from wastewater into aquatic products require
further assessment before wider application of this
technology at the field level.
Substrate/Periphyton Technology
The principle of periphyton-based aquaculture is to
increase the natural food production (both autotrophic
and heterotrophic) by adding hard substrate materials
into the water column (Figure 11). In a traditional fish

pond, phytoplankton is the most important component
for energy fixation and fuelling the food web. However,
phytoplankton-based production can be unstable, with
cycles of algal blooms, crashes and oxygen depletion
leading to inconsistent water. Installing hard substrates
may improve overall nutrient efficiency by stimulating the
periphyton loop. Many fish species can graze on the 2D
layer of sessile food items more efficiently compared to
filter feeding micro-plankton from the water column
[102]. It is also evident that periphyton mats improve
pond water quality through trapping suspended solids,
organic matter breakdown, ammonium and nitrate
uptake and nitrification enhancement [103107]. Another
advantage of periphyton compared to phytoplankton is
that after dying, dead cells remain attached with the
substrates, providing a rich source of organic nutrients
for heterotrophic micro-organisms associated with periphyton layer [108]. Processing of this organic matter
yields inorganic nutrients that can be utilized by living
algae again.
The nutritional quality and energy contents of periphyton are comparable to phytoplankton and suitable for
both herbivorous and omnivorous fish species (Table 2).
Periphyton in nutrient-rich aquaculture ponds contains
relatively higher levels of organic matter and lower ash
14
Figure 9 Concurrent rice-sh ngerling production in the north-west Bangladesh. A farmer is showing brood tilapia (Photo
by M. M. Haque)
content than in periphyton from nutrient-poor open

waters. Under optimum grazing pressure by fish, the
periphyton quality was even better [69]. The quality
varied even within the same substrate types, depending on
the management practices [25]. This suggests that it might
be possible to control the nutritional quality of periphyton
by manipulating the nutrient content and other aspects of
the production environment. This is an interesting area
for future research with, as a first step, research on the
combined effects of nutrient concentrations and ratios on
periphyton composition and productivity. Phosphorous
and nitrogen should certainly be accorded priority,
although it may also be important to consider silicon (Si),
which is a major constituent of diatoms [109]. It is also of
interest to assess the value of periphyton largely dependent on heterotrophic organisms as nutritional quality is
known to be high in a preliminary study conducted in
indoor tanks [110].
Based on a periphyton productivity estimate of
2.22.8 g AFDM/m2/day, Azim et al. [20] estimated a
theoretical fish production of 5000 kg/ha/yr through the
addition of a substrate area equivalent to 100% of the
pond surface area. If there were no tradeoff between
periphyton and phytoplankton productivities in the same

pond, this fish production would be an extra production
on top of the production based on phytoplankton
productivity. There was a negative correlation between
phytoplankton and periphyton chlorophyll a in fertilized
aquaculture ponds without fish, but the tradeoff seems
to be unlikely in ponds where continuous grazing on
phytoplankton and periphyton occurred by the fish [111].
In recent years, the concept of periphyton-based
aquaculture were tested and applied in monoculture
[112, 113], polyculture [79] cage aquaculture [114],
shrimp culture [115] and abalone culture [116], with a
varied degree of dependence on periphyton as food or
substrates as shelter for cultured animals. For freshwater
finfish, the reported increase in production associated
with the use of substrates ranged from 30115% in carp
monoculture and 30210% in carp polyculture, depending
on amount and types of substrates used, cultured
species, nature of ponds (on-station or on-farm) and
other management aspects (e.g., feeding and/or fertilization, etc.). So far, an annual maximum production of
9 t/ha was reported from periphyton-based polyculture
ponds without any supplementary feed [69].
15
Figure 10 Wastewater-fed sh pond in peri-urban Hanoi, Vietnam (Photo by P. Nguyen)
Periphyton technology has also been tested for rearing

two brackishwater finfish species: grey mullet (Mugil
cephalus) and milkfish (Chanos chanos). Growth of grey
mullet was 35% higher in ponds provided with bamboo
poles as periphyton substrates compared to control
ponds without substrates [117]. The growth rate was
even higher (by 73%) for milkfish due to addition of
bamboo poles in saline groundwater ponds [118].
In Israel, a periphyton-based approach is being evaluated for an organic tilapia production in polyculture
[119]. Among other restrictions imposed by organic
standards, fish stocking densities must be low and only
organic feeds and manures must be supplied. Organic
pelleted feeds cost twice as much as regular aquaculture
feeds [119], which reduces economic viability greatly.
Using submerged plastic surfaces equivalent to 40% of
the pond surface area for periphyton production led to
significant improvements in the efficiency of formulated
feed use within tilapia polyculture.
Only relatively few species have been tested in
periphyton-enhanced production systems, and the continued screening of potential culture candidates is needed.
With our present state of knowledge, the selection
of successful species combinations for periphyton-based
polyculture systems [79] is a trial and error process, with
many unknowns. Important factors to consider include
stocking density, size, species ratios, substrate density

and fertilization type, level and frequency. The welfare of
culture animals in periphyton-based system is also an
important issue. There have been reports that periphyton
biofilms have a probiotic function in short-duration
hatchery or larval systems [120, 121], but so far, strong
evidence that probiotics will also work in grow-out
operations is lacking and the issue needs to be investigated.
Periphyton may also have an important role in maintaining water quality in more intensive systems such as
RAS. Sereti et al. [122] compared a conventional RAS with
a periphyton-based RAS system. An illuminated periphyton culture reactor was used in place of a conventional
biological filter producing Nile tilapia (Figure 12). The
periphyton mat was harvested at weekly or biweekly
intervals by scraping the upper side of the grid. Both
growth and nutrient (N, P) retention were superior in the
periphyton-based system compared to conventional RAS.
One promising aspect of this technology is that the
periphyton mat can be harvested at regular time intervals
and fed, with or without processing, to the culture
organisms. Interesting research questions relate to the
harvesting interval, the methods of processing and
feeding of periphyton material, and to the optimum
rations to use.
16
Figure 11 Earthen experimental sh pond at Faculty of Fisheries, Bangladesh Agricultural University provided with
bamboo substrates for periphyton development (Photo by M. E. Azim)
Activated Suspension Technology (AST)

Microbial protein is generated in ponds or other aquatic
systems when organic matter is decomposed by microbial
organisms such as bacteria and protozoa under aerobic
conditions. Such heterotrophic production is an important component of fed and fertilized systems stocked with
micro-particulate feeding fish but is limited by the need
for constant aerobic conditions. The AST, recently
referred to as biofloc technology (BFT) depends on the
use of constant aeration to maintain high levels of bacterial floc in suspension to allow aerobic decomposition
[123] (Figure 13). The technique is based on the idea
that the well-aerated water can contribute to its own
purification in aquaculture systems. Under this condition,
dense micro-organisms develop, functioning both as a
bioreactor controlling water quality [124], and as a
protein food source for the fish [125]. However, the
decomposition process is greatly influenced by the carbon
to nitrogen ratio (C : N) of the organic substrates. The
adjustment of the C : N ratio can be done by manipulation
of the C : N ratio in feed and/or application of carbonaceous substrates to the system [126]. Considering the
C : N ratio of bacterial cells is 5 : 1 [127] and they need
some extra carbon for respiration, the optimum C : N
ratio of the substrates might be increased to 10 : 1 under
aerobic condition. The C : N ratio in an aquaculture

system can be increased by adding different locally available cheap carbon sources (for review see Hargreaves
[128]) and reduction of feed protein content.
The AST seems to be a relatively cheap and simple way
to intensify aquaculture. The fact that water is purified
within the system itself eliminates expenses related to
biofilters or external water-cleaning structures, or reduces the storage capacity required for natural purification in any reservoir. One of the biggest advantages of
this technology over conventional phytoplankton-based
production is that the microbial production is organic
matter/substrate-limited giving rise to the potential
for this system in light-limited situations. However, the
impacts of the inherent high turbidity levels based on the
suspended particles in the water column in activated
suspension systems on the growth and welfare of culture
animal needs assessment.
Although the concept of the AST in intensive aquaculture was derived in the early eighties [129], the
knowledge base concerning the technique is undeveloped.
So far, some fragmentary research works have been
carried out on shrimp farms especially for water quality
management. Very little information is available on the
suitability of AST for finfish species which can utilize
microbial protein as food. Recently, Hargreaves [128]
Trickling
filter
Conventional RAS
Air
Sump biofilter
Pump
Fish tank
Sump
Sedimentation
Periphyton-based RAS
Air
Periphyton reactor
Pump
Fish tank
Sump
Figure 12 Schematic overview of the components of

a conventional RAS and a periphyton-based RAS
(reproduced from Sereti et al. [122] with permission from
European Aquaculture Society)
reviewed the ammonia dynamics, design and operational

considerations, advantages and disadvantages and commercial and experimental applications of suspended
phytoplankton growth (SPG) systems, which are defined
as those for which the maintenance of water quality
depends on an active mass of phytoplankton, free and
attached bacteria, aggregates of living and dead particulate
organic matter, and microbial grazers that is maintained in
suspension. These systems include conventional ponds,
where processes related to the metabolism of phytoplankton have the primary influence on water quality, to
various intensive pond, tank and raceway systems, where
a combination of autotrophic and heterotrophic microbial
processes regulate water quality. Here, we confine our
discussion in those systems where in situ produced
microbial protein is utilized by fish and at the same time
water quality is maintained within the rearing units.
The nutritional quality of microbial protein when used
in standard diets has been established even for carnivorous species such as rainbow trout (Oncorhynchus mykiss)
for which up to 25% replacement of animal protein has
been proposed [130]. For herbivorous species such as the
tilapias it might be expected that microbial protein, being
part of the natural diet, might form a more important
proportion of the diet. Avnimelech et al. ([124] established that biosynthesis and utilization of microbial protein
by the blue tilapia (Oreochromis aureus) could be managed
in culture systems resulting in fish fed lower protein diets
showing identical performance as those fed conventional
17
high protein pellets. Further work [126] showed that

carbohydrate addition promoted nitrogen removal from
the water through synthesis of microbial proteins. The
relationship among the addition of carbohydrates, the
reduction of ammonium and the production of microbial
proteins depends on the microbial conversion coefficient,
the C : N ratio in the microbial biomass, and the carbon
contents of the added material. The addition of carbonaceous substrate was found to reduce inorganic nitrogen
in tilapia commercial-scale ponds. Substitution of part of
the feed protein was possible, leading to reduction in feed
costs by 35%. However, there would be extra costs for
carbohydrates and energy for aeration, which need to be
included in the cost-benefit analysis.
Water use efficiency can also be improved greatly
through use of AST compared to conventional intensification. Milstein et al. [131] compared water quality
and fish growth in conventional intensive ponds with
significant water exchange (500% daily), with active suspension intensive ponds in which water exchange was
very limited (28% daily). The fish tested were two
commercially important species in Israel: hybrid tilapia
(O. niloticusO. aureus) and hybrid bass (Morone saxatilis
Morone chrysops). Bacterial development and nitrification
were greater in the activated suspension ponds. Hybrid
bass and hybrid tilapia performed similarly well in both
types of pond, indicating the economic advantage of
culturing them in the water-saving activated suspension
system. Tilapia fed on suspended particles, leading to
additional savings in feed costs.
In fact, activated suspension systems are modifications
of conventional phytoplankton-based systems emphasizing
the role of bacterial processes. Interactions between
bacteria and phytoplankton contribute to the complexity
of water quality dynamics in these systems. Phytoplankton
and bacteria have a range of stimulatory and inhibitory
effects on each other [132]. There are clear trade-offs
associated with dominance by phytoplankton or bacteria
[128]. Research efforts are needed on possibility of
eliminating the autotrophic processes and complete
reliance on heterotrophic processes. This would allow
application of the technique in indoor, light-limited
systems. The elevated particulate solids concentrations,
characteristic of AST systems might be expected to affect
gill efficiency and other aspects of fish welfare and the
optimum range of total suspended solids for optimal
performance and fish welfare for specific culture animals
needs to be established. The quality and quantity of in situ
biofloc as fish food in relation to floc development and
stability, amino and fatty acid profiles, manipulation of
nutritional quality, etc. need to be evaluated. Interactions
between biofloc and supplementary feed are unknown.
Energy transfer efficiency between biofloc and cultured
animals need to be quantified.
The additional costs related to aeration and mixing
culture systems will need to be understood in comparison
to conventional RAS and traded off with a practical design,
18
Figure 13 Activated suspension indoor tank stocked with Nile tilapia (Photo by F. Murray)
and possibly management of AST systems. These advantages potentially increase its applicability to a wider
range of contexts than investment, technology and management intensive RAS. These and other questions will
require the coordinated efforts of teams of investigators,
consisting of aquaculture engineers, ecologists, nutritionists, microbiologists, and commercial collaborators
to develop a robust technology [128]. The status of AST
and RAS in terms of qualities that might be certified as
organic or sustainable is also important to investigate
further, as these qualities increasingly affect the value of
the product.
Concluding Remarks
There are growing consumer perceptions, especially in
developed world, that organically produced food products
are safer and healthier for both human beings and the
environment. This emerging public preference has created
a global organic food market growing at almost 20%
per year [133]. Global organic fish production is said to
be currently only about 18 000 tons per year, mainly

comprising Atlantic salmon and marine shrimp [134].
One of the main difficulties of organic aquaculture is
that fish feeds must be organic in origin. This strongly
limits the use of the main sources of protein used in
conventional aquaculture feeds and increases the cost of
feeds produced organic. On the other hand, organic
standards encourage the use of feed sources of biological
origin not suitable for human consumption [135]. The
natural food-based aquaculture practices described in this
review seem to conform or could be modified to conform
to the emerging criteria for ecological [136] and organic
aquaculture [135, 137, 138].
Application of novel IMTA, periphyton and AST might
be suitable options in intensifying aquaculture and to
achieve comparable performance to that using formulated
complete feed based RAS. However, the cultured fish
needs to be able to utilize in situ food particles, as is the
case with tilapia. The high-value fish species, normally
cultured in intensive systems, need to be tested in
these new aquaculture systems. As an alternative, in situ
produced natural food can be used as ingredients in
pelleted feed for culturing high-value fish species

if the quality of the natural food seems comparable
with high protein pelleted feed. These approaches could
also be applied to reduce the costs, both in terms
of resource use and environmental impact, associated
with intensification of conventional semi-intensive pond
culture.
There are some limitations in intensifying aquaculture
completely based on the natural food, the application
of supplementary feed is needed not only for further
increase in fish production but also for in situ fish food
production, since uneaten feedstuffs would be used as
substrates for heterotrophic production. However, the
role of supplementary feed in aquaculture ponds is still
not fully understood, the maximum limits of supplementation and its interactions with natural food need to
be quantified. Although polyculture is an age-old practice,
the underlying synergisms are not yet determined.
Despite the fact that periphyton mats efficiently purify
water quality in RAS, more research is needed to
further optimize the functioning of periphyton mats in
periphyton-based RAS in relation to waste loading within
the system. There is a knowledge gap regarding whether
nutritional quality of the periphyton and phytoplankton
can be improved in earthen ponds by manipulating
nutrient inputs. Development of high-quality microbial
floc in activated suspension system by manipulating C : N
ratio of organic substrates is of high interest to intensify
aquaculture. The maximum production limits of microbial
floc, their size, stability and composition should be
determined for better management of this system.
Screening of suitable fish species for this novel technology
and their welfare is a prerequisite before applying the
technology on a commercial scale.
19
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Acknowledgements
The project is funded by the European Commission
through the Marie Curie Incoming International
Fellowship (EC Contract No. MIFI-CT-2005-008965,
ASPECT) and combined with the UK Research Councils
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CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2006 1, No.

Intensifying aquaculture production through new approaches

CABI Publishing 2006 (Online ISSN 1749-8848)

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

Objectives, Scope and Methodology

Overview of Aquaculture Production,

These systems were first developed in countries with

M. E. Azim and D. C. Little

Figure 1 Relative nsh production and degree of

Complete formulated diet

Contribution of formulated diet (%)

Global production (million tons)

Natural supplemental food

Figure 2 Global meat and aquaculture production and

Feed-driven systems, however, are inefficient if feed

Improving the resource efficiency of aquaculture

Ecology of Pond Aquaculture

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

Natural Fish Food: Quantity and Quality

autotrophic and heterotrophic organisms. Three key

M. E. Azim and D. C. Little

Table 1 Reported net primary productivity (NPP) of sh ponds

ash free dry matter basis (AFDM).

mainly on the available inorganic nutrients and sunlight.

plants and detritus has highly variable, but significantly

Increasing Productivity in Aquaculture Ponds

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

concentration was found to be the most suitable nutrient

carbonates. The immediate goal of liming is to neutralize

Herbivorous and Omnivorous Fish Species and

M. E. Azim and D. C. Little

Table 3 Adaptations to herbivory

External taste buds on

To search and select food

barbels (e.g. cyprinids) or on the lips and buccal cavity

semi-intensively cultured organisms range from 2835%

Potential Fish Production Based on Natural

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

and difficulties in maintaining steady productivity due to

Requirement for Feed Supplementation

common goal for any aquaculture system and ponds are

M. E. Azim and D. C. Little

need to increase the crude protein and micronutrient

Manipulating Production Systems

in pond systems are very diverse. The different spatial

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

[82] based on experiments carried out over a duration

Integrated AgricultureAquaculture (IAA) Systems

products and, most crucially, in many contexts to widen

M. E. Azim and D. C. Little

such as lotus (Nelumbo mucifera), can remove significant

Nevertheless, understanding nutrient efficiency in

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

M. E. Azim and D. C. Little

The use of waste stabilization pond effluent within IAA

into the water column (Figure 11). In a traditional fish

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

content than in periphyton from nutrient-poor open

periphyton and phytoplankton productivities in the same

M. E. Azim and D. C. Little

Figure 10 Wastewater-fed sh pond in peri-urban Hanoi, Vietnam (Photo by P. Nguyen)

Periphyton technology has also been tested for rearing

stocking density, size, species ratios, substrate density

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources