Aquaculture

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M. Troell, N. Kautsky, M. Beveridge, P. Henriksson, J. Primavera, P. Rönnbäck, C. Folke and M. Jonell,
Aquaculture, In Reference Module in Life Sciences, Elsevier, 2017, ISBN: 978-0-12-809633-8, http://dx.doi.org/
10.1016/B978-0-12-809633-8.02007-0
© 2017 Elsevier Inc. All rights reserved.

Aquaculture
$
M Troell, Beijer Institute, Stockholm, Sweden and Stockholm University, Stockholm, Sweden
N Kautsky, Stockholm University, Stockholm, Sweden
M Beveridge, Worldfish Center, Lusaka, Zambia
P Henriksson, Leiden University, Leiden, The Netherlands
J Primavera, Southeast Asian Fisheries Development Centre, Tigbauan, Philippines
P Rönnbäck, Uppsala University, Uppsala, Sweden
C Folke, Stockholm University and Beijer International Institute of Ecological Economics, Stockholm, Sweden
M Jonell, Uppsala University, Uppsala, Sweden
r2017 Elsevier Inc. All rights reserved.
Glossary
Aquaculture The farming of aquatic organisms, including
fish, mollusks, crustaceans, and aquatic plants. Farming
implies some sort of intervention in the rearing process to
enhance production, such as regular stocking, feeding, or
protection from predators. Farming also implies individual
or corporate ownership of the stock being cultivated
(Definition by FAO).
Broodstock Fish or shellfish from which a first or
subsequent generation may be produced in captivity,
whether for growing as aquaculture or for release to the wild
for stock enhancement.
Ecosystem service Ecosystem services are the benefits
people obtain from ecosystems. These include provisioning
services such as food and water; regulating services such as
flood and disease control; cultural services such as esthetic
and recreational, values; and supporting services, such as
nutrient cycling, which maintain the conditions for life
on Earth.
Farming intensity In a broad continuum, extensive
systems are those which are closest to natural fisheries,
requiring minimal inputs and offering relatively low yields,
whereas intensive systems require a large amount of inputs
to maintain an artificial culture environment, with high
yields. Between these extremes are the varying degrees of
semi-intensive aquaculture, where definitions are less
distinct: (1) extensive aquaculture does not involve feeding
of the organism, (2) semi-intensive aquaculture involves
supplementation of natural food by fertilization and/or the
use of feeds, and (3) intensive aquaculture is when the
culture species is maintained entirely by feeding with
nutritionally complete diets.
Feed conversion The efficiency of farmed animals to
incorporate given feed into biomass. Feed conversion is
usually expressed in terms of the feed conversion ratio of
weight of feed provided to fish/shellfish flesh biomass
harvested. The ratio is affected by the relative moisture
content of both feed and aquaculture product as well as by
the metabolic characteristics of the farmed species, farming
techniques, and husbandry.
Life cycle assessment (LCA) Environmental framework
incorporating the whole production chain with the
intention of (1) producing an inventory of the economic
and environmental inputs and outputs to each stage of a
product/service life cycle and (2) quantifying a subset of the
environmental impacts potentially associated with those
flows using standardized impact assessment methods.
Seed A term used to describe eggs, larvae, postlarvae, or
juveniles (fry and fingerlings) stocked into aquaculture
production systems.
Spawner Mature individual of a stock responsible for
reproduction.
Introduction
Aquaculture, the aquatic counterpart of agriculture, has grown rapidly in recent decades, and today it produces almost as much fish
and shellfish as fisheries (FAO, 2014). Aquaculture is the main means for obtaining more food from our aquatic environments in
the future. Impacts of aquaculture on biodiversity arise from the consumption of resources, such as land (or space), water, seed,
and feed, their transformation into products valued by society, and the subsequent release into the environment of greenhouse
gases and wastes from uneaten food, fecal, and urinary products, chemotherapeutants as well as microorganisms, parasites, and
feral animals. Negative effects may be direct, through release of eutrophicating substances, toxic chemicals, the transfer of
pathogens diseases and parasites to wild populations stock, and the introduction of exotic and genetic material into the envir-
onment, or indirect through loss of habitat and niche space and changes in food webs. Today, large quantities of fish are caught to
produce fishmeal and fish oil (16 mmt in 2012, FAO, 2014)–an important source of ingredients for protein and fatty acids in
☆
Change History: April 2016. M. Troell added new author and updated author affiliation. Updated text throughout the article, additional text added to section
“Aquaculture Development and Practices,”and added new Figs. 2 and 4 and new section “The Role of Eco-Certification.”References updated and new
references added.
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feeds for many fish and shrimp species. The volume for non-food usage is slowly shrinking but the still high demand from the
aquaculture industry may lead to unsustainable fishing practices with potential negative consequences for fish stocks and marine
food webs (Cao et al., 2015). Despite advances being made within the feed industry, resulting in decreased feed conversion ratios
and development of suitable alternatives to fish resources, the aquaculture industry's use of global fishmeal and fish oil increased
three-fold between 1992 and 2006 (Hasan and Halwart, 2009).
The life cycles for most aquaculture species have been successfully closed but the culture of some, especially marine, farmed fish,
and shrimp, is still partially dependent on the capture of larvae, postlarvae, or gravid females from the wild. This can result in both
over-fishing and bycatch, representing losses to capture fisheries and biodiversity. Large areas of critical habitats such as wetlands and
mangroves have historically been lost due to the siting of aquaculture developments and pollution, resulting in reduced biodiversity
and recruitment to capture fisheries. Today the values of coastal wetlands are better recognized and regulations make it difficult for
large-scale aquaculture development in sensitive coastal areas (eg, mangroves, seagrass beds) in most countries.
The magnitude of biodiversity loss from aquaculture development generally increases with scale, intensity of resource use, and net
production of wastes. In some cases aquaculture may also increase local biodiversity, for example, when ponds are constructed in
dry areas, through re-stocking activities and from integrated aquaculture. Its role in maintaining cultural diversity must also be
acknowledged.
Aquaculture Development and Practices
The farming of aquatic plants and animals is several thousands of years old. Nevertheless, it must be regarded as a largely post-
World War II phenomenon. In 1950, global farmed fish and shellfish production was approximately 2 mmt (million metric tons)
and largely confined to areas of Asia. During the last three decades, aquaculture production has increased by approximately 7–11%
per year. Aquaculture production for 2012 was approximately 44 mmt of finfish, 6 mmt of crustaceans, 15 mmt of mollusks, and
23.8 mmt of aquatic plants (FAO, 2014). Fish produced by aquaculture now accounts for half of all fish directly consumed by
humans although the bulk of this production is freshwater fish (64%, mainly carps) and mollusks (22%, oysters dominating).
Around 600 different freshwater and marine animal species, representing different trophic levels, are cultured using a wide range of
technologies and inputs (Table 1). However, despite the immense diversity the cultivation of fish and shellfish in aquaculture
systems is now dominated by B35 species that together account for 90% of total global production. Four species alone (grass carp,
silver carp, Indian carps, cupped oysters) account for B30% of global aquaculture output by volume (FAO, 2014).
Aquaculture typically involves the enclosure of a species in a secure system under conditions in which it can thrive. Interventions
in the life cycle range from exclusion of predators and control of competitors (extensive aquaculture) to enhancement of food supply
(semi-intensive) or even the provision of all nutritional requirements (intensive). Intensification of production also implies
increasing the number of individuals per unit area, which decreases the local demand for land/sea space but instead requires greater
use and management of inputs, management of waste products and a greater reliance on technology and fossil energy.
Aquaculture is an economic activity that uses and transforms natural aquatic resources into commodities valued by society and
in so doing it may impact on biodiversity, essentially due to the consumption of resources, the transformation process (aqua-
culture), and the production of wastes (Naylor et al., 2000;Boyd et al., 2005;Diana, 2009;Fig. 1). Looking at the diversity of
farming systems it is easy to appreciate that the biophysical impacts of aquaculture activities, that is, magnitude and spatial scale,
Table 1 Summary of the most important aquaculture species groups, farming systems and methods in terms of production
Group System Method of culture
Plants
Eucheuma, Kappaphycus, Gracilaria, Gelidium, Caulerpa Stakes, rafts, long-lines, beds Extensive
Bivalve mollusks
Oysters (Crassostrea, spp.), mussels (Mytilus spp.), Cockles, Abalone Rafts, long-lines, stakes, beds,
tanks
Extensive
Shrimps and prawns
Shrimps (Penaeus spp., Litopenaeus vannamei)Ponds Extensive, semi-intensive, intensive
Marine, brackishwater fish
Milkfish (Chanos chanos), yellowtail (Seriola spp.), groupers
(Epinephelus spp.), mullets (Mugil spp., Liza spp.), cobia
(Rachycentron canadum)
Ponds, cages Semi-intensive, intensive
Freshwater/diadromous fish
Chinese carps, Indian carps, tilapia, Atlantic salmon (Salmo salar), trout,
catfish (Pangasius)
Ponds, cages, tanks Extensive, semi-intensive, intensive
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vary enormously. Technical and economic inputs, such as construction materials and energy, in many traditional aquaculture
systems form only a small part of the inputs needed. The main and critical inputs are instead natural resources and to some extent
also labor. Together with ecosystem services these ultimately determine the limits for the local and global expansion of aqua-
culture. The magnitude and type of resource use and impacts of aquaculture are, however, very much dependent on species
cultured, farming system, intensity of farming methods, and management.
Production practices and their impacts on aquatic ecosystems vary widely across species. Mollusks such as scallops and mussels
are generally farmed along subtidal or intertidal coastlines where wild-caught or hatchery-reared seed are grown in bags set on the
sea bottom or on stakes and suspended ropes. The animals rely entirely on prevailing supplies of plankton and organic particles
for food. Even though no feed is added, large densities of filter-feeding organisms may cause reversible local organic accumulation,
resulting in negative effects on benthic diversity, and possibly also, if farmed in large quantities, impact on pelagic plankton
communities. A range of systems –ponds, tanks, or cages –are used to farm finfish. The majority of carp and other freshwater
species farmed in the tropics and subtropics are herbivores/omnivores and are grown in ponds fertilized by supplemental feeds.
In contrast, most diadromous and marine finfish, including both tropical and temperate species, are farmed intensively in floating
net cages and are to a large extent reliant on nutritionally complete fishmeal and fish oil-based diets. For some marine fish species
farmed mainly in Southeast Asia, including also freshwater species like Pangasius catfish (eg, in Vietnam) large amounts of fish, so-
called trash fish, are being used directly as feed (Huntington and Hasan, 2009).
Penaeid shrimps, dominating crustacean farming, are reared in semi-intensive or intensive coastal pond systems. The shrimps
depend mainly on formulated pellet feeds, aeration to replenish dissolved oxygen, and pumped seawater to dilute pollutants and
flush out harmful metabolites. Shrimp postlarvae are either derived from captured wild spawners/broodstock or directly collected
from the sea –something that is true also for the freshwater shrimp Macrobrachium (Ahmed et al., 2010).
The aquaculture process in itself may affect biodiversity as a result of disturbance through increased road and boat traffic. High
densities of farmed fish and food often attract predators and scavengers such as wild fish, gulls, and seals. These can come into
conflict with farmers and may be killed, either accidentally (entanglement in nets) or deliberately (shooting and trapping), or if
they become established they may displace sensitive local species (Boyd et al., 2005).
Feed Resources
Extensive or semi-intensive aquaculture, for example, pond farmed carps and filter-feeding bivalves, depends either on natural
production or agricultural wastes and some generally locally made feed. Even if filter feeders like mussels do not depend on
addition of feeds dense farming in semi-enclosed coastal areas may impact on the food web. In Rio Arosa, Spain, for example,
overgrazing of the phytoplankton population by filter-feeding mussels resulted in zooplankton starvation and the subsequent
collapse of the sardine fishery (GESAMP, 1991).
Nutrient-rich materials added to stimulate the growth of algae and other food items, and on-farm feeds, based largely on cheap,
locally available agricultural by-products, augmented by household scraps and perhaps small amounts of fishmeal, are used to
supplement the food in extensive ponds. However, in the intensive production systems that predominate in temperate aqua-
culture, and are increasing in the tropics, the farmed animals are to varying degrees reliant on nutritionally complete commercial
feeds containing fishmeal and fish oil. Marine fish species and shrimps have high demand for fish resources in the feed but also
Fig. 1 Diagram illustrating the principal direct and indirect effects from aquaculture on biodiversity, through the use of resources and the
generation of wastes. It should be noted that additional impacts associated with specific culture systems exist, and that as impacts resulting from
management are not included. Note that other impacts being specific to system. Details are given in the text.
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freshwater fish species like carp, tilapia, and catfish, which being herbivores or omnivores, are also increasingly being farmed using
formulated feeds containing various percentage of fishmeal and fish oil (Tacon and Metian, 2008). In 2010, up to two-thirds of the
world’s farmed finfish and crustaceans were dependent on commercial pelleted diets (Tacon and Metian, 2013).
Diets for salmonids, seabass, sea bream, and other carnivores are largely composed of fishmeal and fish oil. Although it may be
possible to replace much of the fishmeal used in intensive fish diets with proteins of plant origin (eg, oilseeds) (Stickney et al.,
1996;Hasan and Halwart, 2009), requirements for essential amino acids, especially cystine and methionine, is still to a large
extent being met by fishmeal. It remains to be seen whether commercial plant protein-based diets can be developed in an industry
in which the product is competing with many others for customer attention and in which profit margins are increasingly being
squeezed. Depending on the source and inclusion rate, oilseed meals can compromise palatability, growth (Stickney et al., 1996),
and profitability. Any decrease in palatability or diet digestibility may aggravate waste loadings to the environment. The issue of
fish oils is even more pressing than that of fishmeal (Naylor et al., 2009). Aquatic carnivores are poor at using carbohydrate to
supply energy requirements, relying instead on protein and lipid (Cowey and Sargent, 1977). The substitution of fish oils with
vegetable oils in freshwater carnivorous or omnivorous fish diets is more straightforward than for marine and diadromous
carnivorous species, such as Atlantic salmon, which require n-3 highly unsaturated fatty acids. Progress has been made with respect
to alternatives sources like rapeseed and linseed as well as synthesis of n-3 fatty acids, which can supplement various feeds while
still resulting in acceptable high growth and quality (Naylor et al., 2009).
Currently, approximately 25% of the total harvest from capture fisheries is destined for nonfood use, of which most is used to
produce fishmeal and fish oil for aquaculture (Tacon and Metian, 2009;Fig. 2). Fish species being used for reduction to fishmeal
Fig. 2 Ecological links between aquaculture and capture fisheries. Thick blue lines refer to main flows from aquatic production base through
fisheries and aquaculture to human consumption of seafood. Numbers refer to 2012 data and are in units of megatons (million metric tons) of
fish, shellfish and seaweeds (green). Thin blue lines refer to other inputs needed for production. Hatched red lines indicate negative feedbacks.
Flows to, for example, pond aquaculture from cage aquaculture also exist as used feed fish generates surplus of fishmeal (not in Figure). Graphic
outline from Naylor et al. (2000). Data from Tacon and Metien (2013) and Matsuoka (2008).
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includes species such as Peruvian and Japanese anchovy, Blue whiting, Atlantic herring, chub mackerel, Chilean jack mackerel,
capelin, European pilchard (Kaushik and Troell, 2010). Many fishes exploited for feed are fast growing opportunistic species and
therefore can sustain a heavy fishing pressure. However, production of some of these species is also constrained by climatic
variability associated with El Nino–Southern Oscillation events (FAO, 1997;NRC (National Research Council), 1999) and
impacts on marine biodiversity from intensive fishing on pelagic forage fish species, including reduction of available food supplies
for marine predators and valuable species consumed by humans, have not been studied in a systematic way (Smith et al., 2011). In
Europe, the crash of North Sea capelin and herring stocks has been attributed to over-fishing and this may have caused depletion
of other wild fish stocks (eg, cod) and the starvation of seals and seabird chicks (Vader et al., 1990;Naylor et al., 2000). Declining
capelin populations in the western Gulf of Alaska are implicated in the decrease of harbor seal and sea lions in the early 1980s
(Hansen, 1997). A strong interaction between anchoveta and seabird and mammal populations has also been well documented
for the Peruvian upwelling system (Pauly and Tsukayama, 1987). Recent focus on fishing for krill near Antarctic for aquaculture
feeds may open up new resources that can be extracted, but as these systems still are not fully understood, and especially how they
will be impacted from climate change, any extraction should be carefully evaluated.
Low value fish, that is, so-called “trash fish”(from rivers, lakes, and the sea) has increasingly been used directly as feed in
aquaculture, especially in Asian countries, with implication for both biodiversity and food security (Huntington and Hasan,
2009). Despite significant progress being made on reducing inclusion of fishmeal and fish oil in feeds, and finding alternative feed
ingredients (eg, plants and microorganisms) (Tacon and Metian, 2008;Naylor et al., 2009), some intensive and semi-intensive
aquaculture systems use more fish protein to feed the farmed species than is ultimately harvested. Also, the increase in global
aquaculture production has resulted in a net increase in total demand for fish resources in aquaculture and it is estimated that 68%
and 98% of global fishmeal and fish oil, respectively, were utilized by the aquaculture sector in 2006 (Tacon and Metian, 2008;
FAO, 2010). Alternatives to fishmeal and fish oil include soy meal, soy oil, livestock co-products, vegetable oil, single cell, and
other locally available resources (eg, snails in Bangladesh). Other commonly used feed ingredients for many freshwater fish species
include rice and wheat bran, maize gluten meal, and cassava meal (Naylor et al., 2009).
In 2006, 74.2% of total aquaculture production was of species feeding low in the aquatic food chain, including aquatic plants,
filter-feeding mollusks, and herbivorous and omnivorous finfish species. Farming of fish species such as carps, tilapia, and catfish
dominates production and even though this production is increasingly based on fish resources, it results in a net production of
fish. This will, however, change if farming methods continue to intensify and increasingly utilize higher quality fishmeal-based
feeds or feeding with low-valued fish (Tacon and Metian, 2009). For other fish species, for example, marine and some diadromous
species (eg, salmon), production requires more fish as feed than is ultimately produced. For example, approximately 3.4 kg of wild
fish is used to produce 1 kg of farmed salmon (estimated IFFO values for 2010 in Tacon and Metian, 2008). The culturing of such
species thus leads to a net loss in fish protein and fish oil.
Human consumption of seafood was 136 mmt in 2012, of which 70 mmt of fish, crustaceans, and mollusks come from capture
fisheries, whereas 67 mmt are from aquaculture (FAO, 2014;Fig. 2). Total capture fisheries was 91 mmt but to this should
approximately 7 mmt of discarded catches be added (Matsuoka, 2008) and of this 22 mmt are being used for fishmeal production
or as direct feed (FAO, 2014). An increasing volume of processing wastes from aquaculture and fisheries are converted into
fishmeal. Even though farming efficiency improves and substitutes for fish in feeds are being developed, an increasing proportion
of fish resources will probably be used for aquaculture feeds as supplies are unlikely to expand and as aquaculture production
continues to grow (and demand for higher trophic level species increasing) and production methods of pond fishes in major
producer countries such as China intensify (Rana et al., 2009).
Land, Water, and Energy
Land is needed to build fish or shrimp ponds or establish tank-based operations, whereas fish cages, pens, and mussel and seaweed
farm operations occupy areas of lakes, rivers, and the sea. Fish ponds are usually sited in agricultural land and this arguably
contributes positively to the floral and faunal diversity of agriculture landscapes. However, unproductive, boggy areas of agri-
cultural land have often been used, and since such boundary ecosystems, or ecotones, may serve as reserves for species in areas
otherwise surrounded by monocultures of crops, this may in fact reduce biodiversity. Land is becoming scarcer and the increasing
competition with other users, for example, agriculture and urban development, puts pressure on aquaculture to minimize
appropriation of land. This has promoted the intensification of farming systems with high stocking densities, resulting in higher
dependence on external concentrated inputs, for example, feed, energy, and chemicals. On the positive side, less land is needed per
metric ton of fish production and the resultant more concentrated wastes are also more amenable to treatment. However, if
treatment is not done the environmental impacts may be severe.
Large areas of tropical coastal wetlands and mangroves have historically been converted to fish and shrimp ponds, resulting in
impoverished biodiversity and recruitment to fisheries, with consequences for local communities and regional economies (Rönnbäck
et al., 2002;Walters et al., 2008). Thus, since the 1400s, hundreds of thousands of hectares of mangroves have been transformed into
milkfish ponds in Indonesia and the Philippines. In recent decades, shrimp farming has been responsible for a significant share of the
conversion of coastal and supratidal areas, for example, 102,000 ha of mangrove forests in Vietnam during 1983–87 (Tuan, 1997)and
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65,000 ha in Thailand during 1961–93 (Menasveta, 1997). When the full range of ecological effects associated with mangrove habitat
loss are accounted for, the net production in fish and shrimp aquaculture may be negative (Rönnbäck, 1999;Barbier et al., 2008).
Coastal ecosystems, such as mangroves, seagrass beds, and coral reefs, provide habitats and nursery areas for many fish and inver-
tebrate species caught in coastal and offshore fisheries (Robertson and Duke, 1987). A positive relationship between commercial fish/
shrimp landings and mangrove area has also been documented throughout the tropics (Pauly and Ingles, 1986;Rönnbäck, 1999). To
identify and value total commercial and subsistence fisheries catch supported by mangroves, economic analyses must take into
account: (1) the large number of resident and transient species that utilize mangroves as habitat; (2) the direct and indirect subsidies of
shrimp trawlers and mangroves, respectively, to total fisheries catch; and (3) the aquaculture industry's dependence on inputs like seed,
broodstock, and feed (Rönnbäck, 1999;Walters et al.,2008). By acknowledging these support functions, the potential life-support
value of mangroves to fisheriesisintheorderof1–10 mmt of fish and shellfish per hectare per year (first sale value E$1000–10,000
US in developing countries) (Rönnbäck, 1999). In addition, mangroves also harbor a wide array of non-marketed fish, crustacean, and
mollusk species, whose subsistence harvest constitutes an important protein source for coastal communities. Different types of
integrated mangrove–shrimp production systems exist in, ie, many Asian countries. Shrimps are here stocked in ponds with mangroves
planted either within the pond or on bunds and/or platforms in and around ponds. These systems are aimed to increase sustainability
within the wider coastal ecosystem (Primavera, 2000;Joffre and Bosma 2009;Troell, 2009). Moreover, mangroves are closely linked to
habitat conditions and associated biodiversity of coral reefs and seagrass beds through the biophysical interactions in the coastal
seascape (Moberg and Rönnbäck, 2003;Nagelkerken, 2009). Almost one-third of the world'smarinefish species are associated with
coral reefs, and fish catches from reefs contribute to approximately 10% of human fish consumption at a global level and much higher
in developing countries (Weber, 1993;Moberg and Folke, 1999).
Aquaculture requires large amounts of water to physically support the farmed animals, replenish oxygen, and remove wastes.
The impacts of aquaculture on the quantity and quality of water resources have direct impacts on associated aquatic biodiversity.
Large amounts of water pass through cages and pens (in the sea or lakes) but there is no net removal from the system. It is
important to distinguish between water consumption and water withdrawal, the former implying that water diverted from
streams, rivers or aquifers lost through evaporation or seepage, while in the latter water is returned to the environment to be reused
or restored (Verdegem and Bosma, 2009). Consumptive water use in aquaculture has mainly impacted on the reduction in
downstream freshwater flows and groundwater resources (Boyd et al., 2005). In land-based systems, aquaculture not only borrows
water, returning it in a more degraded form, but also consumes it or accelerates its loss from surface to groundwater or the
atmosphere (Boyd, 2005;Boyd et al., 2005). Thus, by creating ponds, especially in areas of poor (sandy/loam) soils or high
temperatures, evaporation and seepage are increased and 1–3% of the fish pond volume may be lost in this way each day (up to 45
m
3
kg
1
produced in ponds) (Verdegem et al., 2006;Dugan et al., 2007). Such losses may be particularly significant in arid or
semi-arid areas of the world, such as Israel, where fish pond design and management practices have had to be changed in order to
reduce surface water losses. Conversely, the incorporation of a fish pond into small rural farms has been shown to improve water
conservation (ie, creating a water reservoir) (Dey et al., 2007). In addition, recent analysis shows that indirect freshwater con-
sumption in aquaculture can be significantly higher than direct consumption (Verdegem et al., 2006). This is because formulated
feeds indirectly consume large quantities of water through crop and livestock production. (Troell et al., 2014;Pahlow et al., 2015).
About 1.2 m
3
of water is needed to produce 1 kg of grain. Fish and crustaceans require less grain compared to other terrestrial
animal production, and even if water consumption through feed is large total freshwater consumption by aquaculture is small
compared to, for example, agriculture. Total freshwater use depends on system and practice but it has been estimated that the
8,750,000 ha freshwater and 2,333,000 ha brackish water ponds for aquaculture consume approximately 429 km
3
year
1
(16.9 m
3
kg
1
), which represents only 3.6% of flowing water globally (Verdegem and Bosma, 2009).
Intensification of the aquaculture sector has led to an increasing dependence on external energy inputs throughout the
production chain. Feed is commonly the main energy demanding source for fed aquaculture systems, while pumping, water
purification and aeration may contribute significantly to “closed”systems (Troell et al., 2004; Henriksson et al., in press).
Transportation, in turn, often accounts for a surprisingly small fraction of energy inputs (less than 1% for Norwegian salmon)
(Pelletier et al., 2009) while holding aquaculture products at warehouses can be an energy consumption hotspot for live organisms
such as mussels and abalone (Iribarren et al., 2010). Cumulative energy demand has been shown to provide a good indicator of
both carbon footprint and ecological footprint while the true environmental consequences related to energy production depend
largely on the energy carrier and country of production (Huijbregts et al., 2010).
Wild Capture of Larvae and Spawners
The farming of shrimp and fish depends on larvae collected from the wild or reared in hatcheries from eggs of wild or farmed
broodstock or spawners (Fig. 2). Although most of the aquaculture industry today relies on hatchery-produced fry and fingerlings
derived from parents bred in captivity, some tropical marine fish and shrimp culture, as well as many freshwater fish, still depends
on capture of wild broodstock or juveniles (ie, India, Bangladesh, The Philippines, Indonesia, etc.). Besides adverse effects on wild
stocks of the target species, large bycatch of other larvae are killed in the process, representing losses to capture fisheries and
biodiversity (Naylor et al., 2000;Ahmed et al., 2010). The quantities of bycatch associated with such wild catches are directly
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proportional to the natural abundance of the target species for culture. For example, milkfish Chanos chanos constitute only 15% of
total fry in inshore collections by seine net (Bagarinao and Taki, 1986). The annual utilization of approximately 1.7 billion wild fry
for stocking in Philippine milkfish ponds in the end of the 1990s (Bagarinao, 1997,1998) corresponded to a loss of nearly 10
billion fry of other fish species. Many shrimp and prawn ponds in India and Bangladesh are still to a large extent dependent on
stocking with wild-caught seed of Penaeus monodon and Macrobrachium rosenbergeii (Hoq et al., 2001;Ahmed et al., 2010). The peak
period for this fishery reached one billion P. monodon seed collected annually in southeast Bangladesh (Dev et al., 1994). Up to 900
fish and other shrimp fry species are discarded for every targeted shrimp being collected from estuarine and coastal waters in
Bangladesh (Ahmed et al., 2010). This is sufficiently large to potentially cause major impacts on biodiversity and capture fisheries
production, but to date remains unstudied.
The development of hatcheries for cultured shrimp and marine fish species (eg, milkfish) has reduced dependence on wild
seed. However, it has also increased the demand for wild-caught mature (spawners) and immature (broodstock) shrimp adults
(Rönnbäck et al., 2003). For example, because the species is rare, wild collection of P. monodon broodstock and spawners can lead
to large amounts of bycatch, with consequences for fisheries and biodiversity.
Impacts of Wastes, Chemicals, Diseases, and Feral Animals
The term “wastes”in the current context is used to mean not only food, fecal and urinary products, and chemicals, but also
microorganisms, parasites, and feral animals that may be introduced and subsequently thrive in aquaculture environments which
may subsequently be released to the wider environment (Fig. 1;Beveridge, 2004;Hargrave, 2005). The release of uneaten food and
fecal and urinary wastes may lead to eutrophication and oxygen depletion, the magnitude of the impact depending on the type
and size of operation and the nature of the site, ecosystem characteristics and assimilative capacity. Local effects from nutrient
release into marine ecosystems, from coastal and near-shore intensive aquaculture operations, especially shrimp pond and fish
cage farming, have been well studied (Islam, 2005). For example, eutrophic conditions from uncontrolled fish pen and cage
operations in Pangasinan, Philippines, included increased ammonia, nitrate, nitrite, and phosphate concentrations, and low
dissolved oxygen levels, leading to a major fish kill in 2002 valued at US$ 9 million (San Diego-McGlone et al., 2008).
Sediment impacts associated with cage farming can be severe, resulting in anoxic sediments where fauna been lost. The effect
on sediments is, however, mainly local and biodiversity will return a few years after production stops. However, studies doc-
umenting more large scale and long-term ecosystem changes from excessive nutrient emissions are few. Avoiding release of wastes,
thereby minimizing environmental impacts, has been one of the drivers toward land-based “closed”production systems. This has,
however, come at the price of higher energy dependency (Henriksson et al., 2012). However, semi-intensive, extensive, traditional,
polyculture, and integrated systems generally assimilate much wastes internally (Beveridge, 2004;Edwards, 2009;Troell, 2009)
resulting in fewer wastes being discharged to surrounding ecosystem.
Chemotherapeutants, including antimicrobial compounds and pesticides, are mainly used in intensive fish and shrimp cultures
to control bacterial, fungal, and parasitic diseases. In shrimp farming, prohibited chemicals may be used due to lack of legislation
or poor implementation of regulations. Farmers also use a range of vitamins, immunostimulants, disinfectants, and che-
motherapeutants and employ chemicals for pond soil and water treatment (Gräslund and Bengtsson, 2001). The impacts of many
of these chemicals are largely unknown. The release of antibiotics into the environment can affect microbial biodiversity and
antimicrobial drug resistance but has reduced hugely in the farmed salmon industry due to the introduction of vaccines (Adams,
2009). Controls on use are increasingly strict, especially for aquaculture products aimed at the European and North American
market (Beveridge et al., 2010), but the controls target mainly the finalized products and not the aquaculture production process.
Impacts of aquaculture operations on biodiversity are strongly linked to introductions of exotic species and strains (Naylor
et al., 2001). Worldwide transfers and introductions of the few preferred shrimp culture species, including P. monodon,Litopenaeus
vannamei, and Marsupenaeus japonicus, were numerous in the early decades of commercialized farming (Kautsky et al., 2000). Such
introductions and transfers may lead to competition with endemic fauna, genetic introgression with local fauna, and introduction
of pathogens and parasites (Naylor et al., 2001). Tilapia have had a long history of deliberate (for aquaculture and fisheries) and
accidental introductions to some 90 countries and territories. However, recent studies suggest that impacts of tilapia introductions
in Asia on aquatic ecosystem structure and function have been relatively small and often outweighed by the socioeconomic
benefits (Gross, 1998;Arthur et al., 2010). Atlantic salmon have escaped from culture facilities both within the geographic range of
wild Atlantic salmon as well as in Pacific waters, and are now found as far north as the Bering Sea and as far south as Chile.
Increasing evidence suggests that escapes may have direct genetic impacts on wild populations through hybridization (Walker
et al., 2006). Larger numbers of escapes also increase the likelihood of hybridization between feral farmed Atlantic salmon and
wild fish in populations that are locally endangered or close to extinction (Slaney et al., 1996;Gross, 1998;Hindar et al., 2006). In
addition to consequences for the population gene pool and fitness, there are many potential ecological impacts associated with
feral fish. Feral Atlantic salmon may compete extensively with wild salmon species for food and space, disturb native spawning
sites, and introduce new diseases and parasites into wild populations (Jonsson and Jonsson, 2006).
The consequence of the large-scale introduction of the shrimp Penaeus vannamei into Asia and the Pacific on biodiversity of
indigenous cultured or wild shrimp populations is still uncertain as insufficient time and research have been conducted on this
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issue and there is therefore a need for caution (Briggs et al., 2004). Recent field surveys in the Bangpakong Estuary in Thailand
(where this species contributed 499% of total 2007 marine shrimp production) show that the species is persistent in the wild, and
the presence of Taura Syndrome Virus (TSV) has been detected in seven local species (Senanan et al., 2010). Moreover, laboratory
studies show that P. vannamei can tolerate environmental conditions in the estuary and seeks food better than some of
the indigenous species. The development of genetically modified species for aquaculture is currently being heavily debated
(Kapuscinski et al., 2007), and of particular interest is the “super salmon”that has been developed by Aquabounty and has just
been approved by the US Federal Drug Administration to be farmed commercially. The animal has a single copy of a DNA
sequence that includes code for a Chinook growth gene as well as regulatory sequences derived from Chinook salmon and ocean
pout (Marris, 2010).
Numerous wild salmon stocks in Canada and Norway have been infested by sea lice, either through the release of juvenile
farmed salmon or large densities of fish cages in coastal salmon migration routes (Krkosek, 2010). The mechanisms and linkages
to farmed salmon in Canada, however, is still being debated (Marty et al., 2010).
Diseases are prevalent in many types of aquaculture, especially in highly stocked, intensive production systems, for example,
Atlantic salmon, marine fish species, marine shrimp, etc. For example, the introduction of shrimp postlarvae and broodstock from
areas affected by the White Spot Syndrome Virus (WSSV) and TSV resulted in the rapid spread of these pathogens throughout most
of the shrimp-growing regions in Asia and Latin America, respectively (Kautsky et al., 2000). A native of Asia, where it has caused
multimillion-dollar shrimp crop losses, the WSSV has also been detected in wild and cultured shrimp in Texas and South Carolina.
The virus was probably introduced by release of untreated wastes from plants processing imported Asian shrimp into coastal
waters and by use of imported shrimp as bait in sport fishing or as fresh food for rearing other aquatic species (Lightner et al.,
1997). Another major shrimp virus, the Infectious Hypodermal and Hematopoietic Necrosis Virus (IHHNV), was probably
introduced to the Americas from Asia through the import of live P. monodon in the early 1970s (Lightner et al., 1999). In the
Philippines, IHHNV prevalence in various wild populations of P. monodon has been correlated with intensification of shrimp
culture methods and with mangrove status (Belak et al., 1999). Higher incidence of viral infection in wild shrimp has been
observed in areas with intensive shrimp farms and severely degraded mangroves.
The multibillion dollar Chilean salmon industry was during 2008 hit by Infectious Salmon Anemia (ISA) virus, resulting in
millions of dead salmon and the layoff of thousands of fish farm workers. The main salmon farming areas in Chile are around
Chiloe Island and this area is now being contaminated. Salmon producers are therefore reducing farm and fish densities as well as
seeking to transfer their businesses further south. Whether the move will be successful or not is uncertain because this area has
previously been almost free of farming operations due mainly to its remoteness and concern for the integrity of the seascape.
Another factor that may compromise the successful translocation of salmon farming to the south is that the ISA virus already
appears to be present in these waters.
In contrast to shrimp and salmon, comparatively few diseases have been reported for carps, tilapia, and milkfish, particularly
from extensive and other low-density culture systems. The current trend toward intensification in rearing ponds and cages,
however, may create stressful conditions through deterioration of water quality, excessive stocking, and polluted water inflow that
predispose the fish to disease. The farming of Pangasius catfish in Vietnam has increased rapidly, reaching more than 1 mmt in
2008, and farming is characterized by holding high densities of fish in the ponds, resulting in increased risks for diseases and heavy
usage of antibiotics (Phan et al., 2009).
Resource Use and Carrying Capacity –Energy Analysis, Ecological Footprint and Life-Cycle Assessment
To reduce the risk of resource constraints and impacts on biodiversity, a shift to aquaculture production systems that use less
valuable resources and emit wastes that do not exceed the assimilative capacity of the environment must occur. There is a need to
recognize and manage nature's life support and its provision of ecosystem services, on which economic development and human
welfare depends. Besides traditional EIA one way of identifying the broader demands for natural resources and ecosystem services
of aquaculture has been to estimate the ecosystem area –the ecological footprint –functionally required to support the activity.
When problems beset aquaculture operations, solutions focus on the pond or cage unit, and the fact that the farm is part of a much
larger ecosystem with which it interacts is generally not considered. Surrounding ecosystems provide the feed, seed, clean water,
and other essential resources and services, including waste assimilation. This unvalued work of nature sets the limits to culture
levels without compromising biodiversity or causing pollution or disease problems. The footprint concept has proven to be very
useful in illuminating the nonpriced and often unperceived work of nature that forms the basis for economic activities such as
aquaculture. It is, however, not a detailed tool for measuring environmental capacity or sustainability in aquaculture, but an
excellent tool for communicating human dependence on life-support systems.
An illustration of how the footprint concept can be used for aquaculture is provided by Larsson et al. (1994). They estimated
the spatial ecosystem support, or footprint, for a semi-intensive shrimp farm in a coastal mangrove area in Colombia. Support
included food inputs, nursery areas, clean water, as well as waste processing and the support area was 35–190 times the surface
area of the farm (Fig. 3). The details of the footprint include: mangrove nursery area required to produce the shrimp seed for
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stocking –up to 160 times the pond area; if located close to the farm, the same mangrove area could also supply natural food
inputs (4.2 m
2
m
2
shrimp pond area) and absorb polluting nutrients (2–22 m
2
m
2
pond area) in the farm effluents; feed
pellets, a major input to a shrimp farm, needed a marine area of 14.5 m
2
to produce the fish, and an additional agricultural area of
0.5 m
2
for the agriculture ingredients used in feed pellets; 7.2 m
2
was needed to provide clean lagoon water to the ponds; and
0.8–2.5 m
2
of forest area per square meter shrimp pond area was needed to sequester the CO
2
associated with fossil fuel
consumption at the farm.
Footprint size changes with farming intensity, that, is, a higher stocking density requires more food inputs and produces more
wastes. However, less intensive production operations stock lower densities of species and thus require larger areas to produce the
same biomass of produce. Pressure on local ecosystems can be reduced to some extent by importing some inputs (eg, feeds) from
other areas and by investing in shrimp hatcheries. Although producing seed in hatcheries considerably reduces shrimp and fish
larvae bycatch that would otherwise be recruited populations exploited by fisheries, it also increases demand for wild-caught
spawners and broodstock (Rönnbäck et al., 2003). Other ecosystem services, however, such as clean water supply and waste
assimilation, must be located close to the farming area. Up to a certain level of farming intensity this may pose little problem, but
the whole operation may collapse when the dynamic carrying/assimilating capacity of the local environment is exceeded unless
extensive and costly water treatment facilities are built. The footprint concept provides an early warning device when the level of
carrying capacity is being approached. Integrated farming technologies that re-circulate resources and wastes within the farm may
be one way of reducing the footprint (Troell, 2009).
Aquaculture has directly contributed to the loss of important ecosystem functions (and biodiversity) through land and seascape
transformation, and also more indirectly through, for example, pollution (Deutsch et al., 2011). However, aquaculture has also
enhanced provisioning services, both in the agriculture landscapes and in the seascape, thus leading to improved welfare through
livelihood diversification. Aquaculture can be a viable substitute for some sectors of today's terrestrial animal production (ie, as an
important source of micronutrients and animal-based protein and lipids), proven to be highly resource consuming (eg, beef
feedlot systems, Troell et al., 2014). The question is how to balance the negative and positive consequences from aquaculture
development. The landscape and seascape are today increasingly being managed for multiple functions and services in addition to
provision of food and fiber, and this requires the integration of ecological and socioeconomic research, policy innovation, and
public education. The recently developed “Ecosystem approach to aquaculture”(FAO, 2010) is an example of a broader systematic
perspective on aquaculture development. This is a “strategy for the integration of the activity within the wider ecosystem in such a
way that it promotes sustainable development, equity, and resilience of inter-linked social and ecological systems,”and could
potentially force changes in human behavior with respect to understanding ecosystems functioning and the need for developing
institutions capable of integrating different sectors at multiple scales.
Life cycle analysis (LCA) is a standardized eco-efficiency measurement framework that is increasingly being used to build
inventories and estimate one or several environmental impacts in aquaculture (Pelletier et al., 2007; Henriksson et al., in press).
Fig. 3 Ecosystem support areas required to sustain a semi-intensive shrimp farm in a coastal mangrove area of Columbia/square meters of
support area needed per square meter of pond area.
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LCA identifies system boundaries at the broadest scale, both temporal and spatial, and is a much more quantitative tool than
Ecological Footprints (Fig. 4). Thus, the width of environmental impacts that can be measured allows for more detailed estimates
of the environmental interactions. Climate change, habitat change, pollution and overexploitation are impact categories com-
monly entailed within the LCA framework (Guinèe, 2002), addressing all major drivers, except invasive species, for biodiversity
loss, identified by the Millennium Ecosystem Assessment (2005).
Integrated Aquaculture
Integrated aquaculture may offer opportunities for the efficient usage of water and utilization of nutrients, and increased pro-
ductivity and profits, providing in a single package practical and creative solutions to some problems of waste management and
pollution (Neori et al., 2004). Thus, the resulting environmental impacts from aquaculture and various resource limitations
(water, feed, energy, etc.) may find their solutions in integrated cultivation techniques (Troell et al., 2004). Traditional inland
aquaculture, comprising diverse systems that use on-farm or locally available resources, are still common in Asia, but they are
increasingly being replaced by industrial-based aquaculture technologies (Edwards, 2009). Traditional polyculture/integrated
systems make efficient use of inputs and generate less waste, thus adding to net food supplies locally and regionally at relatively
minor environmental and social expense. Traditional pond cultures of herbivorous fish species (eg, carps in China) have been
viable for centuries and their existence is the proof of sustainable integrated farming systems. Here, raising poultry and livestock is
integrated with fish farming, and the principal linkages between the systems are animal manure and other agriculture waste
products. Compost is used to fertilize the pond water for proliferation of natural organisms as natural feeds for fish from juvenile
to adult. However, despite its environmental advantages the increased global demand for food cannot be met by traditional
extensive production systems (due to demand on space and to low productivity). Even though technological development and
improved management has resulted in increased efficiency and environmental performance of some intensive single species
aquaculture systems, we need to ask what information embedded in traditional integrated systems might be useful for aquaculture
Fig. 4 Illustration of system boundaries being identified in Life Cycle Analysis of an aquaculture production system.
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development. This information could then be added to recent research on integrated aquaculture systems. Integrated aquaculture
is certainly not a panacea for aquaculture development, but should be looked upon as one potential approach among many others
facilitating sustainable development.
The concept of ecological engineering has gained interest in an aquaculture context, with negative environmental effects being
remedied by species integration for nutrient trapping or recirculation. The recent development and promotion of integrated
aquaculture in coastal areas has focused on modern integrated approaches, mainly from temperate and subtropical regions
(China, Canada, South Africa, the Mediterranean Sea, ie, IMTA systems (Integrated Multi-trophic Aquaculture)) involving inte-
gration of fish, seaweeds, crustaceans, and mollusks (Chopin et al., 2002;2008;Neori et al., 2004; ). Such systems try to tackle the
throughput characteristics of many farming systems, in which large amounts of wastes are released to the environment. Thus, in
addition to output of particulate wastes, aquaculture also releases dissolved nutrients, and generally less than one-third of
the nutrients added through feed will be removed through harvest in intensive fish and shrimp farming (Hargrave, 2005;Islam,
2005). Treatment of effluents usually involves a high degree of technology, and therefore high costs, which implies that release
of untreated water is the rule rather than the exception (especially in many developing countries). Besides the improved
environmental performance, the benefits from integration include economic gains resulting from co-production of different
products.
Tropical integrated mariculture systems involve various types of polyculture, sequential integration, temporal integration, and
different integration with mangroves (Troell, 2009). An example of the latter is the use of mangroves as biofilters to process effluents
from aquaculture ponds. Results from the central Philippines indicate that 1.8–5.4 ha of mangroves are needed to assimilate nitrate
wastes from 1 ha of shrimp pond (Primavera et al.,2007). Mangroves and aquaculture are not necessarily incompatible and guides
for responsible use of mangrove areas for aquaculture have been developed (Bagarinao and Primavera, 2005;Primavera et al.,2009).
However, any development of aquaculture within or nearby mangroves needs to be carefully evaluated to identify net benefits and
impacts on environment, biodiversity, ecosystem services, and implications for a variety of stakeholders.
The Role of Eco-Certification
During the last two decades, a number of eco-certification schemes for farmed seafood have been developed. The programs were
developed partly due to a perceived failure of conventional public policy programs to address negative environmental impacts from
the growing aquaculture sector. Presently around 5% of global aquaculture production is eco-certified (Bush et al., 2013), but the share
is expected to grow with Aquaculture Stewardship Council (ASC) covering more producers and species groups the years to come. It
however remains to be seen to what extent eco-certification initiatives can address key environmental impacts and stimulate better
practices among certified producers. It has been suggested that a larger share of the world production of farmed seafood needs to be
certified in order for the mechanism to have a substantial effect on the world’secosystems(Jonell et al.,2013). A major hurdle to be
overcome is that species preferred in Asia, for example, carp, currently are not targeted by the largest certification programs. Exclusion
of small-scale producers (eg, Belton et al., 2011) and a limited coverage of relevant environmental impacts (Jonell et al., 2013)are
other barriers toward obtaining significant environmental and ecological effects from eco-certification.
The scientific evidence of positive effects of aquaculture certification on biodiversity is scarce. One explanation is that aqua-
culture eco-certification is a relatively new phenomenon and environmental effects of implementation of market based instru-
ments such as certification could take decades to manifest. Another reason, applicable also to other sustainability standards, is that
eco-certification programs are providing practice-based instead of performance oriented directives to producers.
Recent research suggest that the prospects of sustainability standards, including aquaculture eco-certification, to have ecological
effects (eg, increasing biodiversity at given locations) could be improved by “spatially explicit ecosystem information”(Chaplin-
Kramer et al., 2015). In order for ecosystem information (hereafter ES information) to be used in certification audits, it needs to be
readily available and easy to use. For aquaculture certification programs, a number of areas where ES information could improve
ecological effectiveness were identified (Chaplin-Kramer et al., 2015). First ES-information could guide where to site re-plantation
efforts of mangrove forest required by eco-certification programs for shrimp aquaculture. Second it could provide direction on the
sensitivity of the surrounding ecosystem on emissions of eutrophying substances and escapes of potentially non-native animals
being farmed. Additionally, information on key ecosystem-services and floral and faunal diversity in a given area would likely be
of great value when conducting site specific Biodiversity inclusive Environmental Impact Assessments (B-EIA) being required by
the largest certification programs for aquaculture.
While earlier work has indicated that eco-certification might be an insufficient tool in reducing loss of biodiversity caused by
aquaculture development, there are also examples of studies demonstrating positive effects of aquaculture eco-certification (Tlusty
and Tausig, 2014). In order for eco-certification of farmed seafood to be a more efficient tool in improving the environmental
performance of the aquaculture sector it is recommended that (1) Asian consumers and markets are targeted in a higher extent
than presently done (Jonell et al., 2013), small scale producers are included (Belton et al., 2011), a life cycle perspective is used to
develop more stringent certification standards (Jonell et al., 2013;Pelletier and Tyedmers, 2008), ecosystem information is used to
support implementation and evaluation of standards (Chaplin-Kramer et al., 2015) and that hybrid forms of governance
mechanisms, including private as well as public instruments, are considered (Bush et al., 2013).
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Conclusions
Since the principle of aquaculture is to reroute flows of energy and matter from the ecosystem into those species that we culture,
aquaculture, like agriculture, will always affect the environment to some extent. This interaction and alteration of supporting
environment is unavoidable, but it should not be done in a fashion that results in the capacity of ecosystems to sustain social and
economic development to be diminished. Recent research has revealed that aquaculture systems are strongly coupled to nature's
subsidies and services to sustain production, and for many species this subsidy expands beyond the local to the global scale.
Conversion of ecosystems, the extraction of feed resources, collection of larvae and broodstock, spread of exotic species,
diseases and effluents, may all add to a spiral whereby total fish supplies are reduced over time. Thus, the real challenge for
aquaculture is to develop farming practices that are in tune with ecosystem processes and functions in a fashion that enhances
aquatic food production. There is great potential to develop techniques that work with nature's dynamics. There is also potential to
redirect unsustainable modes of production into practices that contribute to and enhance nature's support capacity not only for
aquaculture but also for other human activities dependent on aquatic ecosystems. There is no doubt that the aquaculture sector
will move in this direction. Governmental policies and institutional frameworks are required that can make such a transition
possible. The internalization of the costs of deterioration of supporting areas caused by farming will create incentives for the
industry to take a more sustainable path (Folke et al., 1994). This should of course be something that all food production systems
(ie, crop, and animal agriculture) strive toward.
The role of the consumers may be critical in shaping farm management practices. Aquaculture products are increasingly traded
through multinational supermarkets that are highly responsive to customer opinion and demands. If farmed aquatic foods
become associated in the public's mind with poor environmental management and its direct effects on biodiversity, then
supermarkets may well refuse to stock the produce. This is today a reality and many labeling schemes are under development (eg,
Aquaculture Dialogue, WWF).
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