Applied Animal Behaviour Science 86 (2004) 205–223

Stress and the welfare of cultured fish

F.S. Conte∗
Department of Animal Science, University of California at Davis, Davis CA 95616-8521, USA

Abstract

Cultured species of aquatic animals span more than five phyla. Animal welfare attention is directed
towards the vertebrates because of the their neural complexity, and is currently focused on the finfish
because of the size and visibility of that segment of the aquaculture industry. The characteristics
of the aquatic environment and their impact on the animal have forced growers to develop cultural
practices designed to control and minimize animal stress. This was not done as a result of social
awareness, but out of necessity to keep fish alive and healthy; and managing stress is a principal key
in ensuring animal welfare. Aquatic farmers are aware of the consequences of fish stress, but have
limited knowledge of the basic biological principles of animal stress and have little exposure to the
linkages between these concepts and the issues critical to animal welfare. Although the industry has
many tools available for monitoring and preventing stress, not all growers have had exposure to the
information that is available or know of its value when addressing issues of animal welfare.
© 2004 Elsevier B.V. All rights reserved.

Keywords: Fish; Stress; Aquaculture; Animal welfare

1. Introduction

Aquaculture is the culture of plants and animals in fresh, brackish and marine waters.
Although aquatic farming is recorded in antiquity (Bardach et al., 1972), its greatest world-
wide expansion has occurred during the past 30 years, driven by the world’s diminishing
natural fisheries coupled with increased demand for fisheries products (Conte, 1996). The
Food and Agriculture Organization’s (FAO) most recent statistics estimate that in 1999
the total international capture fisheries was about 92.3 million metric tons and aquaculture
production estimated at 32.9 million metric tons (Anon, 2002). Asia, the Indian Subcon-
tinent and Southeast Asia dominate aquaculture production; however, Europe and the US
are significant producers of aquaculture products.
Aquaculture is considered to be a segment of agriculture and, like terrestrial animal
agriculture, is also subject to social attitudes that impact regulations, marketing and product
∗ Tel.: +1-530-752-7689; fax: +1-530-752-7817.
E-mail address: [email protected] (F.S. Conte).

0168-1591/$ – see front matter © 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2004.02.003
206 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

Table 1
Example of cultured aquatic organisms with associated taxa
Kingdoms Examples
Planta Micro- and macro-algae and other aquatic plants
Animalia Invertebrate and vertebrate animals
Animal Phyla Examples

Echnodermata Sea urchins

Annelida Polychete worms, blood worms
Arthropoda Lobsters, crayfish, artemia
Molluska Oysters, clams, mussels, abalone
Chordata Fish, amphibians, reptiles

acceptance. In the past decade, aquaculture has rapidly expanded, and is now recognized as
a major food production industry. As is true for other segments of agriculture, aquaculture
practices are now being examined to assess their impact on the environment and animal
welfare. This paper will address aquaculture practices relative to the major concepts of
animal stress and welfare.

2. Species diversity

Terrestrial animal production uses primarily domesticated species, comprising varieties

with genetically selected production traits. Aquaculture involves hundreds of species that
are only now undergoing the process of domestication, and more often with little or no
knowledge of the specific biological and environmental requirements of the varieties within
species. Farmed aquatic species encompass two biological kingdoms and include hundreds
of species of plants and animals (Table 1). Cultured aquatic animals encompass five major
phyla. Many aquatic species; however, fall outside of the scope of animal welfare concerns
because of the lack of complexity of their neural anatomy and associated physiological
systems. Concepts of animal welfare are generally applied to species with a higher level of
cognition and the associated ability to experience pain and suffering (see Chandroo et al, this
issue). Animal welfare-related research is thus focused on the vertebrates. In aquaculture,
primary attention is on finfish species, because of their neural complexity, and most certainly
because of the size and visibility of the industry. Less attention has been directed towards
the amphibians and aquatic reptiles relative to aquaculture because most of these species
are still captured from wild populations, and the culture industry is relatively small, or lacks
visibility.

3. Finfish production systems

3.1. Facilities and water resources

Finfish production systems are variable in design and degree of intensification (Table 2),
and are intimately linked to water characteristics in terms of quality, quantity and
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 207

Table 2
Examples of finfish production systems with basic descriptions (modified from Beleau, 1990)
Ponds Earthen excavations consisting of a soil or lined, usually irregular, rectangular
or square-shaped water basin enclosed by earthen levies with little water
exchange
Tanks A circular or rectangular rearing unit that is often portable as a whole unit, or
in sections
Open raceway A linier, single water pass rearing unit that is significantly longer than wide
Multiple reuse system A system of tanks or raceways arranged in series enabling water exiting the
first unit to enter the next unit
Closed system A production system in which water is reconditioned by a series of biological
and mechanical filters and continuously recirculated through the system; no
new water added except to make up for evaporative loss
Recycle system A production system in which water is reconditioned by a series of biological
and mechanical filters, continuously recirculated through the system, and a
percentage (10–20%) of fresh water is exchanged with the original water each
day
Silo system A cylindrical, vertical raceway tower usually with a single water pass
Cage system Small or moderate sized net or screen enclosures containing fish that are
usually located in a pond or canal system; and either floating, attached to a
pier, or attached to the bottom
Pen system Large floating net structures suspended from a floating work platform located
in large lakes, bays and open ocean

temperature. Commercial aquaculture facilities require abundant water of the correct quality
and temperature both at the initial source and in the production system. Variations beyond
acceptable ranges for these water parameters lead to stress, distress, impaired health, and
mortality (Conte, 1992). Hatchery personnel are especially attentive to spawning range
temperature requirements because temperature-related stress can impede or eliminate re-
productive performance (Donaldson, 1990; Pankhurst and Van Der Kraak, 1997). The im-
pacts of stress related to water quality and fish health and performance are well documented
(Schreck and Li, 1991). Although stress is inherent to all life, the object of stress manage-
ment is maintaining the level of stress below the threshold of prepathological manifestation
(TPM) (Moberg, 1985, 2000).
Water characteristics in fish culture are affected by factors such as the type of production
system employed, fish density, and the amount and type of food. In natural systems, fish
cages may be located in marine, brackish water, or lakes. Water quality is maintained in
the cage by the sheer volume of water exchange resulting from water current, tide, or by
moving the cages between locations. In recycle production systems, water temperature and
chemical parameters such as oxygen, carbon dioxide, alkalinity, calcium hardness, ammonia
and nitrogen content are controlled mechanically or biologically to maintain water quality
(Masser et al., 1999). Ponds, flow-through tanks and raceways rely on different amounts of
water exchange and aeration to maintain water quality.
Chemical imbalances in water cause direct harm to fish by disrupting such physiological
functions as ionic regulation, gill and kidney function, or by destroying the fishes’ mucous
coating, which is a primary protection against pathogenic and parasitic invasion (Post, 1987;
Klontz, 1993). Some initial chemical deficiencies such as insufficient calcium hardness may
be corrected through supplements added to the fish ration (Tucker and Robinson, 1990).
208 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

Each species of fish has specific requirements for water temperature that are influenced by
genetic variations. Temperature ranges for survival, growth and reproduction in commercial
fish are species-specific and well defined (Piper et al., 1982; Wedemeyer, 1996). The water
quality parameters for culturing coldwater and warm fish species are well documented
for ponds (Boyd, 1981, 1990; Tucker and Robinson, 1990), raceways (Piper et al., 1982),
intensive tank culture (Brune and Tomasso, 1991; Wedemeyer, 1996, 1997) and recycle
systems (Huguenin and Colt, 1989; Brune and Tomasso, 1991; Wedemeyer, 1996, 1997).

3.2. Intensive and extensive systems

Aquaculture production systems may be described either as extensive systems em-

ploying low animal density in relation to water volume, or intensive systems, in which
higher animal densities are used. These are relative terms. Pond production systems are
often referred to as extensive systems; however, many pond production systems are op-
erated at high animal density and more accurately referred to as semi-intensive, or in-
tensive pond systems. In extensive pond culture, water is added primarily to compensate
for evaporation and seepage, and aeration used during periods of hot weather, or when
oxygen levels approach emergency conditions. Intensive pond culture requires additional
water exchange and supplementary aeration. The point of transition between extensive
and intensive pond culture is not exact and the terms are subjective. In general, exten-
sive pond systems are operated at low fish density and require few external resources,
and intensive pond systems require significant resources to support a high-density popu-
lation of fish. Fish density for both extensive and intensive pond culture is expressed as
the biomass of fish per surface area of the pond, for example, 5604 and 13,450 kg/ha,
respectively.
In extensive pond culture, maintaining water quality depends on the pond’s natural ability
to recondition the water. This is accomplished primarily through microbial activity of the
sediment to remove ammonia and carbon dioxide, renewal of oxygen by phytoplankton,
and by atmospheric gas exchange; all of which can be balanced by using animal densities
and feeding protocols that do not overwhelm these natural processes (Boyd, 1990). If an-
imal density and feeding are increased beyond the natural limits of the pond’s ability to
compensate, external resources such as increased water flow and supplementary aeration
become standard procedures to maintain the pond’s water quality. Increasing animal density
results in a greater need for external resources, which leads to concepts of intensive culture
(Table 3).
As pond density approaches the limit in animal carrying capacity, a major limiting factor
becomes the nitrogenous waste product of the fish and the incomplete aerobic nitrification
of ammonia. Nitrite accumulation in the blood of fish results in oxidation of the heme-iron in
hemoglobin from the ferrous to ferric state resulting in a product called methemoglobin, or
ferrihemoglobin, which is not capable of combining with oxygen (Schwedler et al., 1985).
As the condition increases, the blood develops a characteristic brown color and loses its
capacity to transport oxygen. To lower the risk of methemoglobinemia, lower densities are
prescribed, or the ponds monitored for nitrite and treated with a salt (NaCl or CaCl2 ) at a
concentration that maintains a molar ratio of NO2 :Cl, which controls the progress of the
condition (Tomasso et al., 1979).
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 209

Table 3
Examples of land-based aquaculture production systems with common stocking density ranges for channel catfish,
rainbow trout and tilapia
Extensive pond-Channel catfisha
Low 3705–4940 fish/haa
Moderate 7410–9880 fish/ha
High 11,100 fish/ha
Topping pond 24,700 fish/ha
Raceway-Rainbow trout-single passb
Low 25–45 kg/m3
High 80–90 kg/m3
Tank-Tilapiac

Flow through 40–60 kg/m3

Recycle 30–50 kg/m3
a Busch (1985).
b Stevenson (1987).
c Conte (Personal Communication).

The ability to provide emergency relief is essential to prevent stress in all types of pond
culture. Both extensive (Boyd, 1981, 1990) and intensive (Tucker and Robinson, 1990)
ponds are subject to oxygen depletion resulting from excessive or temporary loss of phy-
toplankton, and emergency equipment is essential to supply supplementary oxygen until a
balanced phytoplankton community is re-established.

4. Monitoring aquaculture systems

Developing cultural practices that reduce stress and its potential harmful effects on fish
production is a shared goal among all aquatic farmers. Stressors that appear insignificant may
have cumulative and long-term effects on fish health (Schreck, 2000). Both the producer’s
degree of skill and available level of resources influence the ability to maintain the animal’s
state of well-being. Due to the difficulty of animal production in the aquatic environment,
aquaculture has had to emphasize cultural practices designed to minimize animal stress.
For the producer, this was done without consideration of social concerns for animal welfare
issues, but rather for the sole purpose of keeping fish alive and growing. These practices
include continual monitoring of both the aquatic animal’s environment and the animal’s
physical condition. Information on the condition of the water is obtained by methods ranging
from hand-held metering and water test kits to sophisticated computer monitoring systems
with associated alarms. Stress management protocols include attention to density, fish main-
tenance and handling, changes in animal behavior, and disease.
A number of visual indicators can be used as early warnings of an impending problem.
The condition of the phytoplankton community in ponds is one of the most frequently used
indicators of pond health. Phytoplankton is essential for oxygen production in pond culture.
Pond water transparency and color are affected by phytoplankton density and species and
are used to monitor the health of the phytoplankton (Boyd, 1981, 1990).
210 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

Another indicator is excessive bird activity over ponds, which occurs when fish are
swimming and “mouthing” near the surface, and is often caused by low oxygen. Other
examples include excessive mucous production by fish, fish flashing at the surface indi-
cating parasitic infestation, and flared opercula indicating gill infection. Whenever fish
change behavior, go off feed, or exhibit lethargic or erratic swimming, it is a sign of
unfavorable conditions, stress, distress or pathogenic condition. When these behaviors
are observed, steps should be taken to determine the cause and initiate corrective
actions.
One of the more dramatic visual indicators of stress in some species of fish is a change in
the color of the integument. For example, striped bass and hybrid striped bass will exhibit
color fading as a result of stress, usually beginning with the striations fading in the head
region, then spreading over the body. All bass are easily stressed during handling, which
causes ionic and osmoregulatory imbalances; however, the condition can be corrected by
treatment with salt (McDonald and Milligan, 1997).

5. Fish disease and parasites

5.1. Stress and disease

The literature addressing finfish parasites and pathology of fish disease and infestation
is immense, and an introduction to fish health issues attributed to environmental stressors,
parasites and virulent and contagious pathogens can be found in publications of Piper
et al. (1982), Post (1987) and Klontz (1993). Infectious diseases and parasite problems
usually result from exposure to contagions and other harmful organisms, many of which
are ubiquitous to most natural surface waters (Conte, 1992). When fish are stressed, their
ability to resist the assault is weakened, and stress is considered a primary contributing
factor that leads to impaired health in cultured fish (Iwama et al., 1997). The ability to
maintain animal health involves animal care protocols used to reduce or eliminate exposure
to harmful agents, and actions to be taken when the TPM is exceeded and a disease event
occurs. Frequent and excessive use of therapeutics and medicated feed are indications of
stock that is continuously exposed to pathogens, parasites, or stressors originating from
poor animal handling protocols and system design.

5.2. Disease and management protocols

The catastrophic events caused by the introduction of contagious pathogens often result
from faulty protocols such as sharing equipment between facilities, or introducing new
fish with no inspections for infectious pathogens. Other incidents can be caused by disease
transmission from bird vectors moving between production units, water sources that harbor
wild fish carrying the pathogens and vertical transmission of the disease from parent to
offspring (Piper et al., 1982; Post, 1987; Klontz, 1993). No matter how the pathogens are
introduced, initial site selection including a protected water source is critical to disease pre-
vention (Conte, 1992). Frequent review and reassessment of facility management protocols
are a defense against stress, and essential to fish health.
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 211

Significant progress has been achieved in understanding relationships between specific

stressors, or combinations of stressors, and specific disease manifestations (Wedemeyer
et al., 1976; Wedemeyer and McLeay, 1981; Wedemeyer, 1996, 1997). This knowledge
of the environmental factors commonly associated with the occurrence of infectious and
noninfectious fish diseases provides opportunities to alleviate recurring disease incidence
by changing management protocols and improving system design to remove the source of
stressors (Wedemeyer, 1997).

6. Fish density

6.1. Production in three dimensions

Aquatic production systems are unique in that the animals utilize a three-dimensional
medium. This becomes especially important in intensive culture in which the fish occupy
most of the space during any time period. Fish density in aquatic systems incorporates more
than just the number of animals confined in a given amount of space. In fish production,
density incorporates the number of fish per unit of three-dimensional space as influenced
by the number of fish or weight of fish per volume of static water, and the fish biomass
per volume of flowing water per unit of time (Beleau, 1990). It is the combination of these
factors that influence water quality and fish to fish interaction, and affect the animal’s
welfare.

6.2. Concepts of animal density

Wedemeyer (1996) and Ellis et al. (2001) describe three different, but interrelated con-
cepts that are essential to understanding density, especially in intensive fish culture. The
concepts are carrying capacity, crowding and fish loading density.

6.2.1. Carrying capacity

Carrying capacity in the ecological sense is defined as the maximum number of fish that
the resource of a particular habitat can support. In fish production, carrying capacity is
usually expressed in terms of the water in a rearing unit and weight loading (fish weight per
unit of water flow), rather than the number of fish. The carrying capacity of a given amount
of water is determined by the oxygen consumption rate of the fish and their response to
ammonia, carbon dioxide and other toxic metabolic waste produced (Wedemeyer, 1996).
Carrying capacity is not a fixed term. Ellis et al. (2001) reports that carrying capacity has
been described in the literature by three expressions: (1) the metabolic loading density
kg/l/min; (2) kg food/day/m3 ; and (3) food/available O2 /l/minute. They also report that
carrying capacity is generally used to refer to the maximum biomass of fish based upon
physiological needs, and therefore ignores spatial needs.

6.2.2. Crowding
Crowding is often loosely described as high fish loading density. It more accurately
relates to the behavioral requirements of the fish for physical space and is expressed in
212 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

terms of the weight density, or weight of the fish per unit volume of water, but not water
flow (Wedemeyer, 1996).

6.2.3. Loading density

Fish loading density is the weight of the fish per unit flow of water (Wedemeyer, 1997).
It differs from carrying capacity in that it addresses both the spatial and physiological
requirements of fish (Ellis et al., 2001). Tolerance to high fish loading is related to, but
different from, tolerance to crowding. The concepts of density (crowding) and loading
factors (carrying capacity of the water, spatial requirements, physiological requirements)
are highly significant biological criteria in intensive culture (Wedemeyer, 1996; Ellis et al.,
2001).

6.2.4. Fish density and welfare standards

Ellis et al. (2001) recognize that the concepts of aquatic animal density are continu-
ously developing. They report that designers of aquatic production systems apply density
equations that are applicable to their particular systems, and the equations may have to
be modified to apply to other system designs. The varied system designs complicate the
development of standards for aquatic production systems. In addition, when determining
maximum use of both water and space, conflict can arise between growers and proponents
of animal welfare if economic considerations are considered paramount over concern for
animal health. Animal density is a primary concern in animal welfare, and the subject of
governmental regulation is often a major issue. If aquatic animal density is regulated, it is
important to ensure that the most efficient and appropriate means of quantifying density
and incorporating environmental factors is chosen. However, an alternate approach to safe-
guard welfare may be the designation of appropriate water quality conditions and behavioral
indicators (Ellis et al., 2001).

7. Intensive container production

7.1. Establishing production density

Animal density in intensive tank culture is managed by varying stocking densities in a

series of tanks, with the highest density set so that growers can react to system problems
and maintain the fish in conditions well below the TPM. Once the maximum density is
established, a series of tanks are stocked at low, medium and high densities. The fish stocked
at lower densities grow faster and are marketed earlier, resulting in a time-spread of fish to
market. During the growing period, fish are also graded to size and redistributed in tanks
according to size to lessen size-based competition.

7.2. Water quality versus social interaction

Debate exists as to whether it is poor water quality or increased negative social interaction
that is the primary cause of compromised welfare when fish are maintained at higher densi-
ties. Ellis et al. (2002) reviewed 48 research papers addressing the effects density on rainbow
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 213

trout. Measures included food intake, food conversion efficiency, nutritional status, growth
rate and size variation, health and condition profile, blood profiles, condition of fins, gills,
spleen and thymus, and plasma cortisol. The authors concluded that increased aggression
as the cause of detrimental effects of density was “inferential”, whereas there was direct
experimental evidence indicating that degradation of water quality was the primary cause
for adverse effects of increased density. However, they also observed species-specific differ-
ences in the response to increasing density. Unlike rainbow trout, Arctic charr (Salvelinus
alpinus), exhibit stress-related behavioral responses at low density; the condition is allevi-
ated as density is increased, then reoccurs when the density exceeds a specific threshold.
The authors suggested that until more definitive research is conducted, the most practical
approach for assuring adequate welfare status is to rely on indicators such as acceptable
water quality, health, and body condition.

7.3. Density in container production

Density-related problems are often associated with intensive tank culture, especially in
recycle systems where the water is repeatedly treated and recycled through the production
system. In intensive culture systems the biomass that a given flow of water can support is
usually first limited by metabolism because this determines the rate of oxygen consumption
and waste production. Behavioral requirements for space are usually the second limiting
factor. Although space is important, it is not usually available physical space (volume) that
impacts growth and animal health, but the availability of the high quality water and flow
rates needed to provide oxygen and dilute metabolic waste (Wedemeyer, 1996).
If precautions are not taken, higher fish densities overload systems with metabolites
thereby leading to stress that exceeds the TPM. Stress may result from a number of factors,
but more often is a result of poor system design that is incapable of maintaining water qual-
ity. A balance between stocking density and system design is necessary or water quality will
degrade to harmful values (Smart, 1981; Busch, 1990; Watten et al., 1991). The engineering
related to recycle systems is exacting. Intensive tank and recycle systems offer the best op-
portunity to control water conditions to meet species requirements. However, because any
failure in the system causes rapid deleterious effects these systems also require safeguards in
their design and construction, such as alarms to signal when water parameters are approach-
ing sub-optimal levels, and backup systems to assure adequacy of emergency response. The
short time period between system failure and animal impairment in high-density fish cul-
ture requires strict management protocols to avoid stress-associated loss. Because of this
producers should avoid operating at absolute maximum carrying capacity.

8. Handling fish

In all food animal industries, handling and transport are often stressful events. In aquacul-
ture, the processes of grading, capturing and transporting fish are inherently stressful (Barton
and Iwama, 1991), and made even more complicated because of the aquatic medium. Teleost
fish maneuver and position themselves using their fins and swim bladder, and are subject
to different gravitational forces than terrestrial animals. In addition, handling fish usually
214 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

requires imposing an intrusive foreign element into the water to corral and catch the fish. If
not done correctly, excessive stress can jeopardize fish welfare.

8.1. Nets and seines

Common fish-handling practices include using seines, nets or hands for moving fish to
new aquatic enclosures. If handling, seining, and netting are not done properly, the activity
disrupts the protective mucous coating and fish scales, thereby increases susceptibility
to parasitic or pathogenic invasion (Post, 1987). To avoid disrupting the mucous coat,
fish-handlers should always use wet hands or wear soft, wet gloves when handling fish. The
appropriate makeup of netting varies with species, and depending on presence or absence
of scales and scale type, either a continuous or knotted mesh should be used. Knotted mesh
can dislodge fish scales resulting in parasitic and pathogenic invasion. Seining soil-based
ponds can also disturb the substrate, and if not done correctly and with proper equipment
can result in adverse water quality (Tucker, 1985; Tucker and Robinson, 1990). Most stress
results from rough handling. All fish-handling processes should be slow and deliberate so as
not to increase the natural avoidance reactions of fish, which can lead to excessive activity
and potential exhaustion. The impacts of fish exhaustion, rates of recovery and their relation
to fish welfare are addressed by Schreck (1981, 1990) and Schreck et al. (1997).

8.2. Lift nets and fish pumps

Distress and injury most often occur when fish are loaded into lift nets and cages, and
lifted from the water. Excessive gravitational weight loading on fish positioned at the bottom
of the net can cause injuries from compression and spine injury from adjacent fish. Load
weight should be adjusted to prevent excessive stress and mechanical injuries. It is often
more efficient and less stressful to move fish between tanks or ponds by moving the water
along with the fish. Although fish can be safely moved and harvested using nets, harvesting
and moving fish in water by use of fish pumps or transfer pipes appears to be the least
invasive means of moving fish. This has been accomplished with crustacean culture (Parker
et al., 1974), and is also a common practice today with some finfish species (Conte, personal
observation).

8.3. Acclimation and timing

When fish are moved, the characteristics of the receiving water should be matched as
closely as possible to the source water. Stress can occur if changes in water temperature
and quality are abrupt, even when values are within the tolerance range of the species;
and definitely when they are outside of the range (Wedemeyer, 1997). To prevent abrupt
changes, the fish can be acclimated by gradual water exchange between the source water
and the receiving water.
Temperature has a profound effect on response to handling. Seining and netting activities
should be performed during the cooler portions of the day, as water has less capacity to
hold oxygen at higher temperatures (Wheaton, 1977; Lawson, 1995). In many large pond
operations in desert areas, seining is initiated at night and finished in the early morning
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 215

to avoid handling fish during periods of extreme daytime temperatures. If fish are handled
during maximum heat, the associated stress often results in mortality in both the short
and long-term. Temperature-related stress can occur any time fish are handled, but fish are
especially vulnerable during periods of summer heat (Piper et al., 1982).

9. Transport

Transporting fish is a multiple-phase operation that should be designed to minimize stress

(Piper et al., 1982). Fish are taken off feed for about 24 h prior to harvest and transport so
that they do not void feces and foul the transport water. They are often kept in holding
tanks during this period, which allows them to recover from any previous handling. Fish
are then transferred to a tanker using lift nets or pumps, driven to and off-loaded at the
delivery location. Transporting fish by tank truck requires special care to ensure that water
quality and temperature requirements are maintained, or even compensated for in the event
of elevation changes, which affect the oxygen holding capacity of water. Contemporary
long distance tankers are insulated and equipped with chillers, carbon dioxide strippers,
anti-foam agents, water buffers, circulation pumps, and oxygen sources. Short-haul tank
trucks are usually equipped with ice, circulation pumps, and anti-foam agents.
Much of the research on stress in fish was aimed at overcoming the challenges of harvest
and transportation. Fish display a wide variation in physiological responses to stress, and
genetic history appears to account for much of the inter-specific variation (Barton, 2002).
Elevations in plasma cortisol can differ by as much as two orders of magnitude among
different species of fish following identical stressors. Therefore, some fish transport easily
and with few precautionary steps taken other than the fundamentals of maintaining water
quality and temperature. Others species require specific precautionary steps to prevent
ionic and osmotic imbalances that result in mortality (McDonald and Milligan, 1997).
For example, species such as striped bass (Conte, personnel observation) and black bass
(Carmichael et al., 1984a,b; Carmichael and Tomasso, 1988) require exposure to pre-salted
water before and after transport to withstand the combination of stressors and fully recover
at final destination.
Fish producers are aware that whenever fish are handled or transported, there is a tempo-
rary decline in weight (Conte, personal communication.) Therefore, they generally avoid
repeated handling and allow fish a recovery period after handling and transport. The fish’s
primary physiological responses to acute netting, handling and transport recover in 6 h to
1 day. However, physiological recovery may take from 10 days to 2 weeks if the stressors
persist, but are not lethal (Schreck, 1981; Schreck et al., 1997).

10. Breeding and reproductive technology

As is true for most animals, stress adversely affects the reproductive performance of
teleost fish (Billard et al., 1981). Commercial growers believe that the process of spawning
fish is stressful, and post-spawn fish are given special feeding and environmental atten-
tion to assure recovery and reconditioning for use as future broodstock (Conte, personnel
216 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

communication). Fish species vary in their reproductive behavior and success when placed
in artificial habitats. Some species such as tilapia reproduce so readily, even under high-
density culture conditions, that systems and culture techniques are designed to retard mat-
uration and spawning events (Belarian and Haller, 1982; Guerrero, 1982). Other species
such as sturgeon require spawning induction and assistance to achieve reproductive success,
even when cultured at the lowest density (Conte et al., 1988). Consequently, different ap-
proaches are used to manage reproduction for different species of fish and some examples
are presented below.
In nature, channel catfish spawn in natural crevices, and the male guards the eggs. In
culture, both sexes are stocked at very low density in pond systems containing dispersed
sheltered spawning habitats and at a higher ratio of males to females. Males and females
form pairs and spawning and fertilization events are controlled by the fish. Eggs or fry are
then collected from the spawning shelters (Busch, 1990).
Wild rainbow trout usually migrate to specific riffle areas in side streams off of larger
bodies of water to spawn. Since it is not practical to duplicate this in production aquaculture,
reproduction of farmed trout is usually achieved by maintaining separate-sex populations
in raceway systems. When ready to spawn, the fish are individually removed, hand stripped
for their eggs and milt, and then milt from several males is used to fertilize the eggs from a
single female (Stevenson, 1987).
Breeding of other fish such as Atlantic salmon more closely resembles that of rainbow
trout. Broodstock are usually maintained in net pens at moderate density, and later each sex
is hand stripped of gametes that are used for fertilization (Sedgwick, 1988) Striped bass
are usually induced to spawn using gonadotropin injections followed by strip spawning.
However, when two mature males and a single mature female are placed in a 5 ft diameter
tank, they will exhibit courtship behavior, which will cause the female to release her eggs
(Harrell et al., 1992; Conte, personal observation).
No research to date has addressed any pain or stress specifically associated with hand
stripping fish for gametes. Hand-stripping is usually performed by holding the fish with the
reproductive vent directed towards a collection vessel, gently arching the fish which causes
release of gametes, or gently stroking the abdominal region towards the vent to achieve
the same results. If the fish are hand-stripped they are usually sedated, a method used to
reduce handling injuries to the fish (Piper et al., 1982). If spawned naturally, no sedation is
used (Piper et al., 1982; Sedgwick, 1988; Harrell et al., 1992). The very act of handling fish
is stressful and this combined with hand stripping undoubtedly makes it a stressful event.
If the fish are not to be immediately slaughtered and are to be used as future broodstock,
post-spawn care should be provided.

11. Humane slaughter

Humane methods for animal slaughter are based on the principle that the animal is killed
quickly with minimum fear and pain. Scientific debate still exists as to whether fish have
the neural capability for awareness, fear and pain. Arguments for both sides of the debate
and comprehensive reviews of the concepts of fish awareness, fear and pain can be found
in Rose (2002) and Chandroo et al. (this issue).
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 217

Unlike culture methods that were developed to minimize stress, slaughter technology
for fish evolved to achieve product quality control, efficiency and processor safety. As
a result, application of slaughter technology varies both regionally and internationally,
but most of the methods described here are used within most segments of the food fish
industry. Slaughter methods include electrical stunning followed by decapitation, blunt
trauma to the cranium, percussive stunning using a captive bolt, “cold stunning” and
dewatering.
Electrical stunning in commercial facilities is accomplished by a variety of methods,
but the most common involves loading fish onto metal plates or grates from which the
water is drained immediately before an electric current is applied to the structure. Other
facilities may apply current to the water or container in which the fish are held. After the
fish are electrically stunned, they are decapitated. Blunt trauma to the cranium is performed
using a club called a “priest”. Percussive stunning is performed with a captive bolt system
in which a hand-held unit discharges a metal plate or rod to the cranium of the animal.
Immersion in ice slurry “cold-stuns” the fish, which leads to asphyxiation. Dewatering is
the process of removing the water from the fish container, which results in asphyxiation of the
fish.
Most of the work addressing humane fish slaughter has been conducted in the United
Kingdom and Europe. Humane assessments of slaughter techniques are based on exam-
ination of fish behavior, indicators of sensibility and indicators of brain stem reflexes.
Comprehensive studies addressing these issues can be found in Kestin et al. (1991, 1995,
2002), Robb et al. (2000, 2002), Robb and Roth (2003) and van de Vis et al. (2001,
2003). In general, methods that rapidly render the fish insensible while maintaining qual-
ity control are preferred. Whole fish and head-only electrical stunning, and percussive
stunning are deemed to be the most acceptable methods of fish slaughter based on
measures of welfare considerations and meat quality. The use of ice slurry and other
methods leading to asphyxiation were reported to be less acceptable (Lines et al.,
2002).

12. Behavioral management

Most research on stress and behavior in fish was initiated in order to understand the
basic biology of wild fish and the effects of stress on the survival of hatchery-produced fish
when released during natural resource enhancement. Although these applications continue
to dominate current research, the growth of commercial aquaculture is leading to more
research on the relationships between stress and behavior and on behavioral management
in food production fish.

12.1. Stress and behavior

Fish producers are more familiar with the causes and consequences of stress-induced
physiological disruption than they are with alterations in behavior. Since stress can ini-
tiate behavioral changes and forced behavioral changes can cause stress, knowledge of
species-specific behavior is critical to ensuring fish welfare. Changes in behavior can
218 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

reflect how a fish is sensing and responding to its environment (Schreck et al., 1997). Fish
behaviors that are known to be affected by stressors include swimming performance, ther-
moregulation, orientation and taxes, avoidance, chemoreception, feeding, predator evasion,
and learning (Schreck et al., 1997).
A variety of stressors have been shown to affect swimming performance, orientation
and taxes. Stress from poor nutrition (Fletcher, 1997), especially in early-stage larval fish
often leads to abnormalities that prevent development of adaptive behavioral responses
to environmental challenges. These include proper swim bladder inflation, which affects
buoyancy, swimming ability and survivability (Davis and Olla, 1992; Olla and Davis, 1992).
Sockeye salmon and tilapia subjected to excessive current or prolonged exercise show altered
swimming performance (Bams, 1967; Kutty and Sukumaran, 1975). Hybrid striped bass
exposed to high levels of carbon dioxide exhibit erratic swimming behavior (Conte, personal
communication). When tilapia are exposed to upper and lower temperature extremes within
their tolerance range, they exhibit significant departures from established norms relative to
swimming performance (Kutty and Sukumaran, 1975). Both bluegill sunfish and Atlantic
salmon show changes in temperature preference when stressed (Beitinger and Magnuson,
1975; Peterson, 1976).
Behavioral changes in response to pathogenic microorganisms and parasitic infestation
have been well documented by the industry and in the scientific literature (Post, 1987).
These include increased activity, flashing at the surface and ultimately decreased activity and
lethargy (Warren, 1991; Thoesen, 1994). Parasitic infestations have also cause leaping and
rolling at the surface among pen held salmon (Furevik et al., 1993). Changes in temperature
preference have been demonstrated in bluegill sunfish (Reynolds et al., 1978) and in tilapia
(Tsai and Hoh, 1995) infected with pathogens.
There is little information that directly addresses the effects of stress on learning ability or
memory of fish, and even less information on its application. In laboratory settings, teleost
fish can be conditioned with various negative reinforcements such as touch, temperature
electric shock and bright lights (Gleitman and Rozin, 1971) Stress has been shown to
interfere with performance of learned responses of coho salmon (Schreck et al., 1997) and
this may be especially critical to return rates in salmon ranching and to the survival of
natural salmon populations.

12.2. Environmental preferences

Fish in their natural habitats exhibit preferences for specific environments. Many hatch-
ery operators have reported the linkage between accommodating for the fish’s behavior
and improvement of culture performance. Trout and some other species of fish are re-
ported to do better when they are maintained in subdued lighting rather than under bright
lights (Conte, personnel communication), and some species of larval fish will capture
live food (Daphnia sp. and rotifers) more efficiently when provided with a dark as op-
posed to a lighter background (Conte, personnel communication). Papoutsoglou et al.
(2000), Papoutsoglou (2001) and Rotllant et al. (2003) demonstrated that the internal
background color of culture tanks and the reflective nature of light often act as stressors
that affect fish, and fish growth can be improved by altering the background color in the
tank.
 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223 219

12.3. Competition for feed

A basic principle in fish culture is to reduce harmful competition among animals. In order
to reduce competition among fish for feed and space, fish are graded to approximate size
and different size classes are held in separate containments. When different size-classes fish
are maintained in the same enclosure, it results in social stress between dominant and sub-
ordinate fish. The larger fish dominate available rations; subordinate fish consume more of
their own carbohydrate reserves and experience a decline in growth (de-Oliveira-Fernandes
and Volpato, 1993). When fish are graded to size to avoid competition, moved between
tanks or transported, they often temporarily experience a drop in feeding rate, resulting in
a temporary decline in growth rate. This initial loss is a result of the stress of moving them,
but if fish are handled properly, they recover and gain weight more rapidly than fish that
have not been separated by size (Schreck, 1981).
Other examples of ways in which culture practices are being altered to influence fish
behavior include methods for presenting the rations to fish and managing the social envi-
ronment of broodstock. Fish may be fed a feed that either floats or sinks. Channel catfish
are primarily bottom feeders, but floating feed is often used to observe the relative activity
and health of fish as they feed at the surface, and to adjust the feeding rate based on what
is consumed in a given period of time (Tucker, 1985). However, if heavy bird predation is
a factor, surface feeding will result in young fish being taken, or larger fish experiencing
stressful avoidance reactions or serious wounds (Conte, personal observation).
Male broodstock rainbow trout are competitive in the presence of females, and therefore
the males are usually maintained in enclosures located upstream from the female pens.
This prevents female pheromones from reaching the males, which will initiate aggressive
behavior among the male trout (Conte, personal communication). Most observations of
social interactions among fish stocks are antidotal reports from commercial producers and
institutional fish managers. Behavioral and social interaction among fish reared in con-
finement can have welfare implications and presents opportunities for additional research
effort.

13. Summary and conclusions

Aquatic farming has distinct advantages and disadvantages with respect to addressing
farm animal welfare. Fish have such specific physical and chemical requirements relative to
the aquatic environment, that when these requirements are not met, the animals are quickly
stressed, and their health and survival jeopardized. Culturing animals in water is far less
forgiving, and potential problems occur more frequently than with terrestrial animal culture.
The inherent advantage of this with respect to animal welfare is that aquatic producers
recognize that controlling animal stress is absolutely essential for their economic success;
and that the development of specific stress management protocols is essential to animal
health and survival.
Aquatic farmers are aware of the consequences of fish stress, but are not as aware of the
basic biological principles of animal stress. They also have little exposure to the linkages
between these concepts and the issues critical to animal welfare. If producers are to succeed
220 F.S. Conte / Applied Animal Behaviour Science 86 (2004) 205–223

in meeting the social and political challenges to aquaculture practices, they will have to
understand and use the tools provided by the science of stress biology and animal behavior.
Educators can assist this effort by demonstrating that by removing stress from the animals
and stressors from the production system, profits can be maintained and legitimate aquatic
animal welfare issues can be addressed.
A significant amount of science-based information regarding fish requirements, aquatic
animal stress and fish behavior is already available. The databases originally established by
fisheries biologists were expanded with the development of commercial aquaculture. Al-
though segments of the industry are already using the databases relative to the species they
culture, additional educational efforts are needed to make the information more widespread
across the industry. These databases are not complete for all aquatic species, but the knowl-
edge of what is needed and the direction of research are established.
Additional resources are also required to support research in the area of aquatic animal
stress and behavior if commercial aquaculture is to meet animal welfare challenges to
culture and animal slaughter practices. Aquaculturists, like their terrestrial counterparts,
will ultimately have to address animal welfare issues if public demand for aquatic products
mirrors the expectations relative to other animal commodities.

Acknowledgements

Sincere thanks are extended to Dr. Joy A. Mench for constructive reviews of earlier
versions of this manuscript.

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