Applied Animal Behaviour Science 104 (2007) 251–264

www.elsevier.com/locate/applanim

Review

Parasites, behaviour and welfare in fish

Iain Barber *
Edward Llwyd Building, Institute of Biological Sciences, University of Wales Aberystwyth,
Aberystwyth, SY23 3DA Ceredigion, Wales, UK

Available online 25 September 2006

Abstract
In this review, three reasons are identified as to why it is important to focus on the role of parasites and the
diseases they cause to understand the interrelationships between behaviour and welfare in fish. First, many
of the behaviours exhibited by fish – including their habitat selection, mate choice and shoaling decisions –
are likely to have evolved, at least in part, to limit exposure to deleterious pathogens, including parasites. If
captive housing during husbandry for research, display or aquaculture purposes constrains a fish’s ability to
undertake its normal adaptive behavioural repertoire, yet does not limit the number of infective parasites
present, then increased exposure to parasites is a likely outcome, and this has clear welfare implications.
Second, because parasites are also known to alter the behaviours of host fish – including their locomotion,
competitive ability and foraging behaviour – then welfare issues that are normally associated with the
captive housing may be exacerbated for infected fish. Finally, since fish harbouring specific parasites often
exhibit characteristic behaviours that may be diagnostic of the presence and/or intensity of infections, the
recognition of such behaviours in captive fish may have applied use as a welfare indicator. In this review, I
highlight the major interactions between parasites, behaviour and welfare for teleost fishes, and suggest
some potentially valuable lines of research that could lead to significant improvements for the welfare of
parasitised, and non-parasitised, fish kept in captivity.
# 2006 Elsevier B.V. All rights reserved.

Keywords: Aquaculture; Parasitic infection; Salmonid fish; Vaccination

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
1.1. The scope of the review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 253
2. The influence of captivity on fish behaviour: consequences for infection susceptibility. . . . 254

* Present address: Department of Biology, University of Leicester, Leicester, LE1 7RH, UK. Tel.: +44 116 252 3462;
fax: +44 116 252 3330.
E-mail address: ib50@le.ac.uk.

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2006.09.005
252 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

2.1. Spatial restriction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254

2.2. Crowding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
2.3. Nutritional limitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
3. Effects of infection on fish behaviour: potential welfare concerns . . . . . . . . . . . . . . . . . . 257
3.1. Impaired sensory performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
3.2. Impaired swimming performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
3.3. Competitive ability and food intake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
4. Behavioural indicators of infection in fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
5. Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261

1. Introduction

Aquatic habitats offer ideal conditions for the maintenance and evolution of parasite life
cycles, and fish that live in natural ecosystems are rarely found to be free from infections (Barber
and Poulin, 2002). By definition, parasites impose fitness costs on their hosts (Bush et al., 2001)
and as such, they form part of a suite of environmental stressors (which also include predators)
that are normally encountered by fishes in their natural habitats. Most fish in natural populations,
therefore, carry a parasite burden that is likely to impact negatively on their health (Huntingford
et al., 2006). Parasites are thus expected to exert considerable selection pressure on host
organisms, and are likely to have played a significant role in the evolution of many aspects of fish
behaviour and ecology. Indeed, it is thought that the existence of parasites and other agents of
disease have played a major role in the evolution of mate choice, ornamentation and even the
evolution and maintenance of sexual reproduction (Andersson, 1994; Ochoa and Jaffe, 1999).
Major advances in the field of fish medicine have led to the development of effective
chemotherapeutants (see Stoskopf, 1992; Noga, 2000, for general reviews), and their use is
generally expected to have significant welfare benefits for fish (although some drugs used to
control debilitating infections may also have side effects that create welfare issues; e.g. Toovey
et al., 1999). Furthermore, the incorporation of immunostimulants into feed formulations (see
Section 2.3, below) to boost the immune responses of fish can provide further protection from
parasites (Gatlin, 2002). However, because fish may be maintained under captive conditions (in
aquaria, tanks or mesh enclosures) for a variety of purposes, it is important to recognise that the
desirability and likelihood of treatment will vary; whereas chemotherapeutants may be used
against unwelcome parasite infections in aquaculture or in display aquaria, in research, infections
may be induced intentionally and little remedial action taken, in order to replicate the ‘natural’
disease phenotype as accurately as possible under controlled conditions. Furthermore, the cost of
treatments and supplements, as well as concerns over the toxicity of some parasiticides (e.g.
Srivastava et al., 2004) and the potential for some compounds to negatively impact native
biodiversity (e.g. Spratt, 1997) may also lead to fish being held without disease treatment.
In most cases, it is therefore probably unrealistic to expect that fishes kept in captivity under
natural or semi-natural conditions (i.e. where infective parasite are capable of accessing potential
fish hosts) to be maintained in a parasite-free condition, and in general, low level infections with
co-evolved parasites within the intensity range normally encountered for the population of origin
are unlikely to raise significant welfare concern. However, if the levels of infection developed by
fish in captivity, if the particular strains or species of parasites to which fish are exposed are
 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 253

changed by the husbandry process, or if husbandry practices alter a fish’s capacity to cope with
(tolerate) normal levels of infection, then parasites may become a welfare issue for captive
housed fish.

1.1. The scope of the review

Clearly, parasites have the potential to directly reduce the performance of their hosts, in terms
of growth and reproduction, through their direct impacts on fish health. However, the direct
effects of parasites on fish hosts are reviewed in detail elsewhere (e.g. Roberts, 1989) and are not
the focus of this paper. Instead I focus specifically on examining the potential welfare
implications of interactions between parasites and the behaviour of host fish (see Fig. 1).
Patterns of individual behaviour and infection status often co-vary and different mechanisms
may generate the observed patterns. Firstly, natural variation in the pre-infection behaviour of
individual fish – which may be related to factors such as age, gender, body condition or genotype
– can lead to differential exposure to infective parasite stages, with behavioural differences
therefore generating the observed variation in infection level. Alternatively, parasite infections,
once acquired, may affect ‘normal’ patterns of host behaviour (Barber et al., 2000), with the
observed behavioural differences being generated by pre-existing variation in infection level.
Behavioural changes that are associated with parasite infections may, in turn, arise because they
confer some fitness benefit on either the parasite (‘adaptive host manipulation’, such as reduced
anti-predator behaviour of fish parasitised by a trophically transmitted parasite; Moore and
Gotelli, 1990) or the host (‘behavioural defence’, such as visiting cleaner fish; Hart, 1990), or
they may be a result of inevitable side effects of infection (Poulin, 1998).
There are consequently three main reasons why it is important to address the role of parasites
in an exploration of the interrelationships between welfare and behaviour in fish. Firstly, the
captive housing of fishes being used for research, display or in aquaculture may restrict the
expression of normally adaptive behaviour patterns, and this could lead – through wide variety of
mechanisms – to elevated infection levels (Section 2, below). Secondly, many of the documented
effects that parasites have on the behaviour of their hosts may exacerbate welfare problems that

Fig. 1. The interrelationships between parasites, behaviour and welfare status in fish. Parasites may affect ‘normal’
patterns of host behaviour [1], either as a simple side effect of the debilitating nature of infections, or because the
behaviour change benefits parasites (‘manipulation’) or hosts (‘cleaning’). Behaviour can also affect an individual’s
exposure to parasites [2], and if captive housing affects normal patterns of behaviour, this may lead to increased infection
levels. Parasites may impact directly on the welfare status of fish held in captivity [3] if husbandry practices lead to an
increase in the level of exposure, or a reduction in the ability of individuals to tolerate otherwise normal levels of infection.
The welfare status of fish may also have implications for susceptibility to infection [4]. The behaviour of fish in captivity
may influence welfare status, for example, if inappropriate feeding regimes generate increased levels of competition
between individuals for food [5]. Conversely, fish welfare status may influence patterns of behaviour [6]. Parasites can,
therefore, influence fish welfare directly, or indirectly by influencing patterns of host behaviour [route 1 ! 5].
254 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

are normally associated with the captive housing of fish (Section 3, below). A third reason is that
fish harbouring high parasite loads sometimes exhibit characteristic behaviours that might serve
as useful indicators for the diagnosis of infection status (Section 4, below).

2. The influence of captivity on fish behaviour: consequences for infection

susceptibility

Being held under captive conditions imposes constraints on fish that potentially impair their
capacity to exhibit adaptive patterns of behaviour, which may include behaviours that have
evolved to avoid or limit exposure to infective parasites, or to actively reduce infection loads
(Hart, 1990). For example, enclosures – such as sea or lake cages – restrict the spatial movements
of fish, potentially limiting the opportunities for fish to select low infection-risk habitats, or to
avoid particular habitat types that are associated with an elevated risk of parasite acquisition.
Foraging opportunities, and hence diet, may also be restricted, limiting any possibility fish may
have of selecting a diet that provides maximum protection against infections. The high densities
of fish held under intensive culturing conditions also preclude natural patterns of spatial
organisation, dramatically reducing inter-individual distances, and increasing the potential for
the spread of parasites that rely on spatial proximity between hosts for transmission. On the other
hand, aquaria frequently lack the presence of required intermediate hosts, reducing the risk of
infection by indirectly transmitted parasites; the use of frozen and/or artificial diets may also
reduce the input of parasites into ‘closed’ systems. In this section, the various constraints that
captive housing imposes on fish behaviour are reviewed with the aim of identifying likely, or
demonstrated, consequences for infection susceptibility.

2.1. Spatial restriction

Experimental studies have suggested that fish can base decisions regarding their spatial
distribution on both the presence of infective parasite stages, and the inherent risk of infection
associated with particular habitat types. Elegant experiments by Poulin and FitzGerald (1988,
1989) showed that sticklebacks Gasterosteus spp. were capable of detecting the presence of
ectoparasitic branchiuran lice (Argulus canadensis) and shifted normal habitat preferences for
specific water depths and vegetation cover to minimise contact with high infection-risk habitat
when lice were present. Recent laboratory trials have also shown that rainbow trout,
Oncorhynchus mykiss, are capable of detecting and avoiding areas with high densities of
infective cercariae of the trematode Diplostomum spathaceum (Karvonen et al., 2004a), with
complementary field studies also demonstrating that higher levels of infection than normally
observed are acquired by fish placed in lake cages close to a source of cercariae. The results of
these studies suggest that if the capacity to modify habitat choice in response to the detection of
infective parasite stages is constrained, then any adaptive behavioural control that individual fish
have over their exposure to parasites may be impaired. This may be exacerbated if locally high
densities of fish lead to their increased detectability by mobile parasites (see Section 2.2, below),
and suggests that the selection of enclosure sites should be considered carefully.
Fish movements over larger spatial scales are also precluded by captive housing, and this may
also have implications for parasite load. During the marine–freshwater transitions of salmonids
and other migratory fish, parasites acquired at sea (such as caligid copepods, or ‘sea lice’) are
typically lost as they fail to cope with the physiological demands of freshwater (Heuch et al.,
2002) and this seasonal loss of some debilitating infections may be a considerable benefit of
 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 255

migration (Wagner et al., 2004). Preventing such transitions in fish housed in large scale, open
cage culture is, therefore, likely to facilitate the build up of infections. Infections can alternatively
be eliminated if salmonid smolts are sourced from freshwater environments and reared in tanks
with filtered seawater, thus eliminating many infective parasites from the system.
Many of the anti-parasite behaviours of fish are reliant on the availability of environmental or
ecosystem components that are unlikely to be available in captivity. Interspecific cleaning of
ectoparasites in fish is widely documented from tropical and temperate marine, and tropical
freshwater, ecosystems, with specialist taxa (typically wrasses and gobies, but also some
shrimps) cleaning ectoparasites from the external surface of host fish (Lowe-McConnell, 1987).
The evolution of cleaning symbioses has been the focus of considerable research (Poulin and
Grutter, 1996), and a recent study – in which the levels of infection with gnathiid isopods
amongst client fish (Hemigymnus melapterus) were studied following the experimental removal
of cleaner wrasses (Labroides dimidiatus) – has demonstrated convincingly that cleaners
significantly reduce the level of ectoparasite infection on host fish (Grutter, 1999). This study
strongly suggests that if infected client fish are maintained in captivity and are unable to elicit the
services of cleaners, then infection levels are likely to increase. Alternative strategies of cleaning,
including jumping, and skin abrasion against hard substrata or nets in cages (Urawa, 1992) may
reduce parasite loads, but such behaviours also incur damage to skin and fins that is likely to
increase the likelihood of secondary microparasite infections (e.g. Clayton et al., 1998).

2.2. Crowding

Parasites are thought to have been important in determining the natural aggregation strategies
of host organisms, and infection status plays a key role in partner and shoal choice, both in a
mating and a social context, in fish (Kennedy et al., 1987; Barber et al., 1995; Krause and Godin,
1996). Fish may be rejected as potential sexual partners or shoalmates as a result of directly
detectable infections (Rosenqvist and Johansson, 1995; Krause and Godin, 1996; Barber et al.,
1998) or because the infections they harbour have intensity-dependent effects on ornamentation
or behaviour (Kennedy et al., 1987; Milinski and Bakker, 1990). Captive housing of host fish at
unnaturally high densities removes individual-level choice of social partners, and hence
potentially negates these evolved strategies of infection avoidance.
There are other reasons why the size and density of aggregations formed by potential hosts
might be expected to affect their risk of acquiring infections, and hence why deviations from
normal patterns of aggregation might generate abnormal infection levels. However, predicting
the direction of the relationship between group size and infection level is not straightforward and
requires an understanding of the transmission strategies of the parasites involved. A meta-
analysis of published data, undertaken by Côté and Poulin (1995), identified consistent positive
correlations between host group size and both the prevalence and intensity of contagious
parasites, but also suggested that larger group sizes may provide dilution benefits against mobile
ectoparasites that are limited to ‘attacking’ single hosts per visit and are not directly contagious.
Crowding of fish held in captivity might influence the level of infection developed through
several mechanisms. First, the size or density of the group may have implications for the ease
with which parasites can locate hosts (Wertheim et al., 2003). Mobile aquatic parasites (such as
the cercariae of diplostomatid trematodes) use chemotaxis to locate potential fish hosts (Haas
et al., 2002; Sukhdeo and Sukhdeo, 2004), so larger and/or more densely packed groups of fish
may be more easily detected by parasites that rely on host olfactory cues for orientation. Second,
for contagious, directly transmitted parasites that require close spatial proximity between hosts to
256 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

spread and are capable of rapid reproduction on individual hosts, larger groups are expected to
increase opportunities for transmission (Alexander, 1974). For ectoparasites that rely on fish–fish
contact (or at least the close spatial proximity of hosts) for transmission, the high densities of fish
under intensive rearing conditions have implications for the establishment and spread of infections
(Pillay, 1993; Sasal, 2003; but see Bagge et al., 2004 who suggest that the total number, and not the
density, of hosts may limit the parasite population). However, although positive correlations have
been identified between infection levels and group size in birds and mammals (Hoogland, 1979;
Brown and Brown, 1986; Moore et al., 1988; Poulin, 1991), the evidence for a similar relationship
in fishes is less compelling (Barber and Poulin, 2002). Thirdly, environmental and social stress
associated with crowding may reduce the capacity of individuals to tolerate otherwise normal levels
of infection. Urawa (1995) demonstrated that although levels of infection with the ectoparasitic
flagellate Ichthyobodo necator amongst juvenile chum salmon, Oncorhynchus keta, remained
unaffected by rearing density, the pathology of infections were significantly increased in high
density treatments, suggesting that social or environmentally induced stress associated with high
rearing densities affected the fish’s capacity to tolerate the parasites. In a recent review of the
relationships between stocking density and welfare in farmed rainbow trout, Ellis et al. (2002)
identify fin erosion – resulting from reduced water quality, aggression or abrasion – as a commonly
reported effect of increased density. Fin erosion may result in an increase in secondary infection by
bacterial, fungal or protozoan pathogens (e.g. Clayton et al., 1998).

2.3. Nutritional limitation

Natural environments present animals with a wide variety of potential foods, and strategies of
diet selection are expected to have evolved that support growth and reproduction at a rate that is
optimal (Forbes, 1995). Consequently, animals that are constrained in their movements as a result
of captive housing are faced with a more limited range of foods and may be unable to make
optimal diet choice decisions. This may have implications for both the level of food intake and
the nutritional composition of the diet. A great deal of research has been undertaken examining
the dietary requirement of fish from the perspective of developing ‘ideal’ diets for growth
performance in common aquaculture species and it is evident that, for example, missing essential
(non-synthesisable) amino acids can lead to reduced growth (Wilson, 2002).
However, food does not only provide ‘fuel’ for growth and development. There is an
increasing body of evidence that diet or dietary components may contribute significantly to fish
health, and nutrient deficiencies can directly affect immune function and parasite resistance
(Gatlin, 2002). Hence, diets that do not provide these components may reduce a fish’s capacity to
withstand parasite invasion or establishment. It has been speculated that selective foraging on
foods rich in carotenoids may be beneficial to animals because of their known anti-oxidant
properties and also because carotenoids may have specific anti-parasite properties (Olson and
Owens, 1998). In fish, the reported consequences of supplementary dietary carotenoids range
from a general enhancement of performance to specific functions in reproduction, metabolism
and antioxidant status (Christiansen et al., 1995; Torrissen and Christiansen, 1995). Recent
research by Amar et al. (2001, 2004) provides evidence that dietary carotenoid supplementation
can increase both humoral and cellular components of the immune system of rainbow trout. The
fact that the inclusion of other immunostimulants – including beta-glucans and fungal derivatives
– into commercial feed formulations can lead to significant fish health benefits (e.g. Sahoo and
Mukherjee, 2003; Rodriguez et al., 2004; Bagni et al., 2005), further supports the suggestion that
inadequate diets may have consequences for infection resistance.
 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 257

More controversial than suggesting that animals naturally select a healthy ‘balanced diet’ is
the proposition that animals might actively seek out naturally occurring compounds in plants,
soils, insects, and fungi to provide specific protection against infections, or eliminate already
acquired parasites (Engel, 2002). Although it remains untested in fishes, and controversial in
other non-human taxa, the potential for self-medication (‘zoopharmacognosy’) remains (Lozano,
1991). Although speculative, removing fish from their natural foraging environments might,
therefore, impose as yet unidentified dietary restrictions that impair their natural capacity to
counter infections.

3. Effects of infection on fish behaviour: potential welfare concerns

As discussed above, certain behaviour changes associated with infection, such as visiting
cleaning stations, may be beneficial to hosts since they reduce parasite levels, and these
behaviours may be viewed as host adaptations to infection. However, other behavioural changes
in hosts may reflect parasite adaptations that increase the probability of successful transmission
or otherwise maximise parasite fitness (Lafferty, 1999). Alternatively there remains the
possibility that some behaviour changes simply reflect inevitable ‘side effects’ of infection that
benefit neither parasite nor host (Poulin, 1998). Differentiating between the various explanations
for infection-associated behavioural change, and generating data on its fitness consequences for
hosts and parasites under natural environments, remains a key challenge for parasitologists
(Poulin, 2000).
However, whether changes in host behaviour that occur after infection are adaptive to
parasites or not, an understanding of the physiological mechanisms by which behaviour is altered
is valuable, and a number of mechanisms are possible (Barber and Wright, 2006). If parasite
infections impair the functioning of peripheral sense organs then the quality and/or quantity of
information obtained by hosts sampling their environments may be reduced. Alternatively, if
infections have significant energetic consequences then parasites may change the internal
nutritional status of fish hosts, and hence the motivational basis to respond to external stimuli.
Furthermore, parasites that physically damage the CNS, manipulate hormone or neurotransmitter
levels, or have neuromodulatory effects may interfere directly with the control of host behaviour.
Moreover, parasites may impact on the capacity of hosts to perform normal patterns of behaviour
in response to perceived stimuli by altering the energetic efficiency of effector functioning
through their effects on respiration, circulation, locomotion or stamina.
If the behavioural effects of parasites lead to a reduction in the performance of their hosts
under captive housing then this may represent another way in which parasites impact welfare of
fish through behavioural mechanisms (see Fig. 1). In this section, the various types of effects
parasites can have on host behaviour are summarised, and examined with the aim of determining
how they may impact the welfare of infected fish maintained in captivity.

3.1. Impaired sensory performance

Parasites can cause local pathology to host tissues by their attachment, movements, growth or
development, and so the specific sites they occupy can have important consequences for the
behaviour of hosts (Holmes and Zohar, 1990). In fish, the eyes, nares, inner ear and lateral line are
common sites of infection for many parasites (Williams and Jones, 1994), which consequently
have the potential to significantly impact the sensory performance of their hosts. The majority of
studies have focused on parasites that impair visual performance, in particular the metacercariae
258 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

of diplostomatid trematodes that invade the lens and/or retinal tissue of a wide variety of
freshwater fish (Chappell et al., 1994). These infections cause extensive lesions that can lead to
cataract formation (Dorucu et al., 2002; Karvonen et al., 2004b), with significant consequences
for the visual performance, foraging and anti-predator behaviour of infected fish. For example, D.
spathaceum metacercariae in the lenses of dace, Leuciscus leuciscus, and three spined
sticklebacks, Gasterosteus aculeatus, reduce host reactive distances to prey (Crowden and
Broom, 1980; Owen et al., 1993) and impair foraging efficiency, with the result that heavily
infected host fish spend more time foraging (Crowden and Broom, 1980). The implications of
these behaviour changes for fish housed in captivity can be serious, with heavily infected fish
being typically emaciated, even under favourable feeding regimes (Shariff et al., 1980; Chappell
et al., 1994). Although the effects of parasites inhabiting other sensory systems are not well
studied, it is possible that those affecting olfaction, lateral line function and electroreception
could similarly impair the ability of hosts to locate food (Barber and Wright, 2006). Furthermore,
if infections impact on learning and memory in fish as they are thought to do in other taxa (e.g.
mice; Kavaliers et al., 1995) then parasitised fish may also fail to learn spatiotemporal patterns in
food availability.
Impaired sensory performance may also affect a fish’s ability to recognise or respond to
predators. The reduced visual performance of Diplostomum infected fish, and the altered time
budgets and spatial distributions that result, increases their risk of predation (Brassard et al.,
1982) and also makes them more susceptible to netting by humans (Seppälä et al., 2004). Of more
relevance to the welfare of fish held under captive housing (where predators are unlikely to pose a
significant threat), impaired sensory systems can also have implications for the ability of
individual fish to recognise individual conspecifics. The recognition of individual conspecifics
coveys significant benefits to fish, including reduced competition, and is a pre-requisite for the
formation of dominance hierarchies (Ward and Hart, 2003). If infected fish are less able to
recognise dominant individuals then they may expose themselves to higher levels of aggression.

3.2. Impaired swimming performance

Parasites can interfere with host swimming behaviour in a variety of ways. The metacercariae
of Diplostomum phoxini and Ornithodiplostomum ptychocheilus, which infect minnows in the
UK and the USA, respectively, appear to achieve their effects via damage to the CNS. The
metacercariae aggregate in lobes of the brain concerned with vision and motor control (Barber
and Crompton, 1997; Shirakashi and Goater, 2002), and heavy infections are associated with
impaired optomotor responses (Shirakashi and Goater, 2002) and ‘conspicuous’ swimming
behaviour of host fish (Ashworth and Bannerman, 1927; Rees, 1955; Lafferty and Morris, 1996).
Parasites that inhabit the heart muscle, live in the lumen of blood vessels or reduce the oxygen
carrying capacity of the blood can impair swimming performance by reducing the efficiency of
the cardiovascular system (Williams and Jones, 1994). For example, the heterophyid trematode
Ascocotyle pachycystis locates in and occludes the bulbus arteriosus of sheepshead minnows
(Cyprinodon variegatus), reducing the time infected fish are able to swim at their maximum
sustainable velocity before becoming exhausted (Coleman, 1993). Anaemia, which is a
commonly reported symptom of infection with blood feeding ectoparasites, also typically
decreases the swimming performance of fish (Gallaugher et al., 1995).
Parasites may also increase the energetic cost of locomotion, exacerbating any intrinsic
energy costs of infection for hosts, if infection alters swimming performance by affecting the
hydrodynamic properties of fish. The isopod Anilocra apagonae negatively affects the swimming
 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 259

behaviour of host cardinal fish (Cheilodipterus quinquelineatus) by increasing drag which can
only overcome by increased pectoral beat frequency, with the resulting increased energetic
expenditure leading to weight loss during periods of food restriction (Östlund-Nilsson et al.,
2005). Similar effects may occur in fish infected with bulky endoparasites, which may also alter
buoyancy or buoyancy control (LoBue and Bell, 1993; Barber et al., 2000).

3.3. Competitive ability and food intake

Nutritional stress in animals maintained in captivity can create a major concern for welfare,
and parasites certainly have the potential to induce nutritional stress in host fish. Studies of
infected fish in natural field populations and under captive housing frequently demonstrate
reduced body condition and/or growth rates in infected individuals (e.g. Gauldie and Jones, 2000;
Ward et al., 2005). Yet in most cases, the causal factors – which are likely to range from impaired
sensory capacity and reduced competitive foraging behaviour through to the energetic drain
imposed by some infections and altered host activity levels – are generally unclear. Identifying
the precise mechanisms by which infections mediate host body condition is challenging, and in
most cases a number of factors may operate. Yet understanding at what level infections are
impacting on host food intake is important so that remedial action can be taken.
Where fish are housed in groups then an individual’s ability to identify, approach and ingest
food items efficiently assumes even greater importance in determining its food intake. Parasites
that impair sensory performance or swimming behaviour, as described above in Sections 3.1 and
3.2, are therefore likely to significantly impact host foraging success in competition with other
less heavily infected individuals. Parasites may also restrict the food intake of hosts if they
physically restrict the capacity of the stomach (Cunningham et al., 1994; Wright et al., 2006) or
prevent normal gut evacuation by blocking the alimentary canal.
Both the level of feeding (ration) and the spatiotemporal distribution of food during feeding
are important determinants of the type of competition that is likely to be generated within groups
of fish. Localised food input, which can generate a defendable resource, may lead to the
formation of despotic competition regimes (Grand and Grant, 1999), benefiting dominant
individuals. Random input type feeding generates scramble competition, benefiting those fish
that are able to locate and approach incoming prey fastest. The type of competition generated can
have implications for the relative performance of infected fish within groups, depending on how
infection affects behaviour. In experiments where three spined sticklebacks infected with
plerocercoids of the cestode Schistocephalus solidus were paired with size-matched, non-
infected conspecifics, Barber and Ruxton (1998) found that infected fish performed better when
multiple food items were presented sequentially than when they were presented together. Under
the simultaneous presentation treatment, infected fish were not able to match the intake rate of
non-infected fish and as a consequence consumed fewer prey, but when food items were
presented at intervals, infected fish were able to compete reasonably well, possibly by
maximising the time spent scanning for food. These results suggest that the feeding regimes
under which fish are maintained may be important in determining the relative performance of
infected individuals.
Even in the absence of competition, individual food intake may drop as a consequence of
parasite infections, but interpreting the proximate and ultimate causes of changes in voluntary
meal size is difficult. Rainbow trout infected with the haemoflagellate Cryptobia salmositica
exhibit a voluntary reduction in feed intake (‘anorexia’), with the level of anorexia being closely
linked to the density of parasite stages in the blood (Chin et al., 2004). Although it has been
260 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

hypothesised that this reduction in voluntary meal size is an adaptive response of hosts
experiencing certain types of parasite infection, since it deprives parasites of nutrients, few
studies have examined the impact of host ration on parasite growth and success. Further research
into the effects of host food intake on the capacity of fish to reduce/tolerate parasite infections
would be valuable (Barber, 2005).

4. Behavioural indicators of infection in fish

If parasites induce characteristic, easily identified behaviours in their hosts then they may
serve as useful diagnostic tools to allow the identification of potential welfare concerns
(Huntingford et al., 2006). Altered host behaviour as a consequence of infection may in itself be
an important criterion for identifying infected fish that are experiencing reduced welfare. A wide
variety of parasites only impact patterns of host behaviour significantly when they attain a certain
size, developmental status or infection intensity, and thus behavioural changes may have value as
sensitive indicators of infections that are attaining levels that make them a welfare concern. For
example, Diplostomum phoxini infection in minnows is associated with altered host swimming
behaviour only in the most heavily infected fish (those harbouring ca. 10 the mean intensity of
infection; Rees, 1955). A similar pattern is seen in killifish, Fundulus parvipinnis, infected with
brain-encysting Euhaplorchis californiensis metacercariae, with increasing levels of infection
being associated with more ‘conspicuous’ behaviours (Lafferty and Morris, 1996). Myxosoma
cerebralis – the protozoan causative agent of ‘whirling disease’, which is of economic
significance in the cage aquaculture of salmonids – destroys the cartilage of the inner ear of host
fish, which subsequently display erratic circular swimming movements, but only severe
infections are associated with behaviour change in the host (Uspenskaya, 1957; Kreirer and
Baker, 1987; Markiw, 1992). For trophically transmitted parasites that influence host behaviour
as a probable adaptation to enhance predation rates by susceptible predators, changes in
behaviour often coincide with parasites attaining infectivity. The impacts of Schistocephalus
solidus infections on the anti-predator behaviour and escape performance of host sticklebacks
thus is only evident once the plerocercoids attain 50–100 mg (Tierney et al., 1993; Barber et al.,
2004). Simple behavioural assays, or behavioural observations, could, therefore, be used as non-
invasive indicators of infection status and welfare of captive housed fish.

5. Future directions

Biologists are now increasingly recognising the importance of the role played by parasites in
animal ecology and evolution, and it is evident that the threat posed by the presence of infective
parasites in the environment has shaped many aspects of the behaviour of fish. The capacity of
parasites to alter the behaviour of their hosts is also becoming increasingly evident, though
interpreting these changes remains a challenge. In this review, I have tried to show how captive
housing potentially alters the capacity of fish to avoid infective parasites through behavioural
mechanisms, and how behavioural changes associated with infection might impact on the welfare
of fish in captivity.
In reviewing the topic, a number of potential areas for research have emerged. Many of the
examples cited are drawn form a rather limited set of ‘classic’ model host–parasite systems. Such
systems are typically chosen for their convenience as experimental systems, because of the small
body size of the host and the ease of housing large numbers of individuals under controlled
conditions. Yet few of these systems have applied importance, and they are often not
 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 261

representative of the host fish that may be kept in aquaculture or in display aquaria, or of the types
of parasites that are likely to most relevant. There is, therefore, a requirement to undertake studies
investigating the interactions between behaviour, welfare and infection in a wider range of host
and parasite taxa.
Our knowledge of the precise interactions between hosts and parasites and the role of
behaviour is also limited by the relatively small number of experimental studies that have been
undertaken. The majority of studies undertaken utilise naturally infected host fish, and the
directional, causal relationships between infection status and behaviour are often very difficult to
identify, and more studies that examine the behaviour of fish following experimental exposure to
parasites are required to elucidate the mechanisms that control behavioural change.
Finally, the relationships between parasite infections, the behavioural changes they cause and
the welfare of host fish deserve more thorough investigation. Studies that incorporate both
behavioural observations and quantitative physiological indicators of stress are likely to be
essential to determine whether behavioural changes caused by parasites are likely to have applied
use as indicators of welfare status.

Acknowledgements

Thanks to Lynne Sneddon for inviting this paper and to Ben Rushbrook and Hazel Wright for
constructive comments.

References

Alexander, R.D., 1974. The evolution of social behaviour. Ann. Rev. Ecol. Syst. 5, 325–383.
Amar, E.C., Kiron, V., Satoh, S., Watanabe, T., 2001. Influence of various dietary synthetic carotenoids on bio-defence
mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult. Res. 32 (Suppl. 1), 162–173.
Amar, E.C., Kiron, V., Satoh, S., Watanabe, T., 2004. Enhancement of innate immunity in rainbow trout (Oncorhynchus
mykiss Walbaum) associated with dietary intake of carotenoids from natural products. Fish Shell. Imm. 16, 527–
537.
Andersson, M., 1994. Sexual Selection. Princeton University Press, New Jersey, 599 pp.
Ashworth, J.H., Bannerman, J.C.W., 1927. On a tetracotyle (T. phoxini) in the brain of the minnow. Trans. R. Soc. Edin.
55, 159–171.
Bagge, A., Poulin, R., Valtonen, E.T., 2004. Fish population size, and not density, as the determining factor of parasite
infection: a case study. Parasitology 128, 305–313.
Bagni, M., Romano, N., Finoia, M.G., Abelli, L., Scapigliati, G., Tiscar, P.G., Sarti, M., Marino, G., 2005. Short- and long-
term effects of a dietary yeast beta-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in
sea bass (Dicentrarchus labrax). Fish Shellfish Imm. 18, 311–325.
Barber, I., 2005. Parasites grow larger in faster growing fish hosts. Int. J. Parasitol. 37, 137–143.
Barber, I., Crompton, D.W.T., 1997. The distribution of Diplostomum phoxini metacercariae (Trematoda) in the brain of
minnows (Phoxinus phoxinus). Fol. Parasitol. 44, 19–25.
Barber, I., Poulin, R., 2002. Interactions between fish, parasites and disease. In: Hart, P.J.B., Reynolds, J.D. (Eds.), The
Handbook of Fish and Fisheries. Blackwell Science, Oxford, pp. 359–389.
Barber, I., Ruxton, G.D., 1998. Temporal prey distribution affects the competitive ability of parasitized sticklebacks.
Anim. Behav. 56, 1477–1483.
Barber, I., Wright, H.A., 2006. Fish physiology and behaviour: the effects of parasites. In: Sloman, K., Wilson, R.W.,
Balshine, S. (Eds.), Behaviour and Physiology of Fish. Fish Physiology, vol. 24. Elsevier/Academic Press, pp. 110–
149.
Barber, I., Huntingford, F.A., Crompton, D.W.T., 1995. The effect of hunger and cestode parasitism on the shoaling
decisions of small freshwater fish. J. Fish Biol. 47, 524–536.
Barber, I., Downey, L.C., Braithwaite, V.A., 1998. Parasitism, oddity and the mechanism of shoal choice. J. Fish Biol. 52,
1365–1368.
262 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

Barber, I., Hoare, D., Krause, J., 2000. The effects of parasites on fish behaviour: an evolutionary perspective and review.
Rev. Fish Biol. Fisher. 10, 131–165.
Barber, I., Walker, P., Svensson, P.A., 2004. Behavioural responses to simulated avian predation in female three-spined
sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour 141, 1425–1440.
Brassard, P., Rau, M.E., Curtis, M.A., 1982. Parasite-induced susceptibility to predation in diplostomiasis. Parasitology
85, 495–501.
Brown, C.R., Brown, M.B., 1986. Ectoparasitism as a cause of natal dispersal in cliff swallows. Ecology 67, 1206–1218.
Bush, A.O., Fernández, J.C., Esch, G.W., Seed, R., 2001. Parasitism: The Diversity and Ecology of Animal Parasites.
CUP, Cambridge, UK.
Chappell, L.H., Hardie, L.J., Secombes, C.J., 1994. Diplostomiasis: the disease and host–parasite interactions. In: Pike,
A.W., Lewis, J. (Eds.), Parasitic Diseases of Fish. Samara Publishing, Dyfed Wales, pp. 59–86.
Chin, A., Guo, F.C., Bernier, N.J., Woo, P.T.K., 2004. Effect of Cryptobia salmositica-induced anorexia on feeding
behavior and immune response in juvenile rainbow trout Oncorhynchus mykiss. Dis. Aquat. Organ. 58, 17–26.
Christiansen, R., Glette, J., Lie, ø., Torrissen, O.J., Waagbø, R., 1995. Antioxidant status and immunity in Atlantic salmon,
Salmo salar L., fed semi-purified diets with and without astaxanthin supplementation. J. Fish Dis. 18, 317–328.
Clayton, R.D., Stevenson, T.L., Summerfelt, R.C., 1998. Fin erosion in intensively cultured walleyes and hybrid walleyes.
Prog. Fish Cult. 60, 114–118.
Coleman, F.C., 1993. Morphological and physiological consequences of parasites encysted in the bulbus arteriosis of an
estuarine fish, the sheepshead minnow, Cyprinodon variegatus. J. Parasitol. 79, 247–254.
Côté, I.M., Poulin, R., 1995. Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. Sociobiol. 95,
159–165.
Crowden, A.E., Broom, D.M., 1980. Effects of the eyefluke, Diplostomum-spathaceum, on the behaviour of dace
(Leuciscus leuciscus). Anim. Behav. 28, 287–294.
Cunningham, E.J., Tierney, J.F., Huntingford, F.A., 1994. Effects of the cestode Schistocephalus solidus on food-intake
and foraging decisions in the 3-spined stickleback Gasterosteus aculeatus. Ethology 97, 65–75.
Dorucu, M., Dilsiz, N., Grabbe, M.C.J., 2002. Occurrence and effects of Diplostomum sp infection in eyes of
Acanthobrama marmid in Keban Dam Lake, Elazig, Turkey Turk. J. Vet. Anim. Sci. 26, 239–243.
Ellis, T., North, B., Scott, A.P., Bromage, N.R., Porter, M., Gadd, D., 2002. The relationships between stocking density
and welfare in farmed rainbow trout. J. Fish Biol. 61, 493–531.
Engel, C., 2002. Wild Health: How Animals Keep Themselves Well and What We Can Learn from Them. Houghton
Mifflin Company, New York, 276 pp.
Forbes, J.M., 1995. Voluntary Food Intake and Diet Selection in Farm Animals. CAB International, Oxford, UK, 532 pp.
Gallaugher, P., Thorarensen, H., Farrell, A.P., 1995. Hematocrit in oxygen transport and swimming in rainbow trout
(Oncorhynchus mykiss). Resp. Physiol. 102, 279–292.
Gatlin III, D.M., 2002. Nutrition and fish health. In: Halver, J.E., Hardy, R.W. (Eds.), Fish Nutrition. third ed. Academic
Press Inc., San Diego, CA, USA, pp. 671–702.
Gauldie, R.W., Jones, J.B., 2000. Stocks, or geographically separated populations of the New Zealand orange roughy,
Hoplostethus atlanticus, in relation to parasite infestation, growth rate, and otolith shape. B. Mar. Sci. 67, 949–971.
Grand, T.C., Grant, J.W.A., 1999. Spatial predictability of resources and the ideal free distribution in convict cichlids,
Cichlasoma nigrofasciatum. Anim. Behav. 48, 909–919.
Grutter, A.S., 1999. Cleaner fish really do clean. Nature (Lond.) 398, 672–673.
Haas, W., Stiegeler, P., Keating, A., Kullmann, B., Rabenau, H., Schonamsgruber, E., Haberl, B., 2002. Diplostomum
spathaceum cercariae respond to a unique profile of cues during recognition of their fish host. Int. J. Parasitol. 32,
1145–1154.
Hart, B., 1990. Behavioural adaptations to pathogens and parasites: five strategies. Neuro. Biobehav. Rev. 14, 273–
294.
Heuch, P.A., Knutsen, J.A., Knutsen, H., Schram, T., 2002. Salinity and temperature effects on sea lice over-wintering on
sea trout (Salmo trutta) in coastal areas of the Skagerrak. J. Mar. Biol. Assoc. U.K. 82, 887–892.
Holmes, J.C., Zohar, S., 1990. Pathology and host behaviour. In: Barnard, C.J., Behnke, J.M. (Eds.), Parasitism and Host
Behaviour. Taylor and Francis, London, UK, pp. 193–229.
Hoogland, J.L., 1979. Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys sp.)
coloniality. Behaviour 69, 1–35.
Huntingford, F.A., Adams, C., Braithwaite, V.A., Kadri, S., Pottinger, T.G., Sandoe, P., Turnbull, J.F., 2006. Current issues
in fish welfare. J. Fish Biol. 68, 332–372.
Karvonen, A., Seppala, O., Valtonen, E.T., 2004a. Parasite resistance and avoidance behaviour in preventing eye fluke
infections in fish. Parasitology 129, 159–164.
 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 263

Karvonen, A., Seppala, O., Valtonen, E.T., 2004b. Eye fluke-induced cataract formation in fish: quantitative analysis using
an ophthalmological microscope. Parasitology 129, 473–478.
Kavaliers, M., Colwell, D.D., Galea, L.A.M., 1995. Parasitic infection impairs spatial learning in mice. Anim. Behav. 50,
223–229.
Kennedy, C.E.J., Endler, J.A., Poynton, S.L., McMinn, H., 1987. Parasite load predicts mate choice in guppies. Behav.
Ecol. Sociobiol. 21, 291–295.
Krause, J., Godin, J.-G.J., 1996. Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanus,
Teleostei, Cyprinodontidae). Ethology 102, 40–49.
Kreirer, J.P., Baker, J.R., 1987. Parasitic Protozoa. Allen and Unwin, Boston, 241 pp.
Lafferty, K.D., 1999. The evolution of trophic transmission. Parasitol. Today 15, 111–115.
Lafferty, K.D., Morris, A.K., 1996. Altered behavior of parasitized killifish increases susceptibility to predation by bird
final hosts. Ecology 77, 1390–1397.
LoBue, C.P., Bell, M.A., 1993. Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its
intermediate host, Gasterosteus aculeatus, the threespine stickleback. Am. Nat. 142, 725–735.
Lozano, G.A., 1991. Optimal foraging theory: a possible role for parasites. Oikos 60, 391–395.
Lowe-McConnell, R.H., 1987. Ecological Studies in Tropical Fish Communities. Cambridge University Press, Cam-
bridge, p. 382.
Markiw, M.E., 1992. Salmonid Whirling Disease. US Fisheries and Wildlife Service Leaflet 17, Washington, DC.
Milinski, M., Bakker, T.C.M., 1990. Female sticklebacks use male colouration in mate choice and hence avoid parasitised
males. Nature (Lond.) 344, 330–333.
Moore, J., Gotelli, N.J., 1990. A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the
manipulation hypothesis. In: Barnard, C.J., Behnke, J.M. (Eds.), Parasitism and Host Behaviour. Taylor and Francis,
London, UK, pp. 193–229.
Moore, J., Simberloff, D., Freehling, M., 1988. Relationships between bobwhite quail social-group size and intestinal
helminth parasitism. Am. Nat. 131, 22–32.
Noga, E.J., 2000. Fish Disease: Diagnosis and Treatment. Iowa State University Press, USA, 367 pp.
Ochoa, G., Jaffe, K., 1999. On sex, parasites, and the red queen. J. Theor. Biol. 199, 1–9.
Olson, V.A., Owens, I.P.F., 1998. Costly sexual signals: are carotenoids rare, risky or required? TREE 13, 510–
514.
Östlund-Nilsson, S., Curtis, L., Nilsson, G.E., Grutter, A.S., 2005. Parasitic isopod Anilocra apogonae, a drag for the
cardinal fish Cheilodipterus quinquelineatus. Mar. Ecol. Prog. Ser. 287, 209–216.
Owen, S.F., Barber, I., Hart, P.J.B., 1993. Low level infection by eye fluke, Diplostomum spp., affects the vision of three-
spined sticklebacks. J. Fish Biol. 42, 512–517.
Pillay, T.V.R., 1993. Aquaculture: Principles and Practices. Blackwell Scientific, Oxford, UK, 575 pp.
Poulin, R., 1991. Group-living and infestation by ectoparasites in passerines. Condor 93, 418–423.
Poulin, R., 1998. Evolutionary Ecology of Parasites: from Individuals to Communities. Chapman and Hall, London, UK.
Poulin, R., 2000. Manipulation of host behaviour by parasites: a weakening paradigm? Proc. Roy. Soc. Lond. B 267, 787–
792.
Poulin, R., FitzGerald, G.J., 1988. Water temperature, vertical distribution, and risk of ectoparasitism in juvenile
sticklebacks. Can. J. Zool. 66, 2002–2005.
Poulin, R., FitzGerald, G.J., 1989. Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can. J. Zool. 67,
14–18.
Poulin, R., Grutter, A.S., 1996. Cleaning symbioses: proximate and adaptive explanations. Bioscience 46, 512–517.
Rees, G., 1955. The adult and Diplostomulum stage (Diplostomulum phoxini (Faust)) of Diplostomum pelmatoides
Dubois and an experimental demonstration of part of the life cycle. Parasitology 45, 295–311.
Roberts, R.J., 1989. Fish Pathology, second ed. Bailliere Tindall, London, 467 pp.
Rodriguez, A., Cuesta, A., Esteban, M.A., Meseguer, J., 2004. The effect of dietary administration of the fungus Mucor
circinelloides on non-specific immune responses of gilthead seabream. Fish Shellfish Imm. 16, 241–249.
Rosenqvist, G., Johansson, K., 1995. Male avoidance of parasitized females explained by direct benefits in a pipefish.
Anim. Behav. 49, 1039–1045.
Sahoo, P.K., Mukherjee, S.C., 2003. Effect of dietary beta-1,3 glucan on immune responses and disease resistance of
healthy and aflatoxin B-1-induced immunocompromised rohu (Labeo rohita Hamilton). Fish Shellfish Imm. 11, 683–
695.
Sasal, P., 2003. Experimental test of the influence of the size of shoals and density of fish on parasite infections. Coral
Reefs 22, 241–246.
Stoskopf, M., 1992. Fish Medicine. W.B. Saunders, Philadelphia, 902 pp.
264 I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264

Seppälä, O., Karvonen, A., Valtonen, E.T., 2004. Parasite-induced change in host behaviour and susceptibility to predation
in an eye fluke–fish interaction. Anim. Behav. 68, 257–263.
Shariff, M., Richards, R.H., Sommerville, C., 1980. The histopathology of acute and chronic infections of rainbow trout
Salmo gairdneri Richardson with eye flukes, Diplostomum spp. J. Fish Dis. 3, 455–465.
Shirakashi, S., Goater, C.P., 2002. Intensity-dependent alteration of minnow (Pimephales promelas) behaviour by a brain-
encysting trematode. J. Parasitol. 88, 1071–1074.
Spratt, D.M., 1997. Endoparasite control strategies: implications for biodiversity of native fauna. Int. J. Parasitol. 27, 173–
180.
Srivastava, S., Sinha, R., Roy, D., 2004. Toxicological effects of malachite green. Aquat. Tox. 66, 319–329.
Sukhdeo, M.V.K., Sukhdeo, S.C., 2004. Trematode behaviours and the perceptual worlds of parasites. Can. J. Zool. 82,
292–315.
Tierney, J.F., Huntingford, F.A., Crompton, D.W.T., 1993. The relationship between infectivity of Schistocephalus solidus
(Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus.
Anim. Behav. 46, 603–605.
Toovey, J.P.G., Lyndon, A.R., Duffus, J.H., 1999. Ivermectin inhibits respiration in isolated rainbow trout (Oncorhynchus
mykiss Walbaum) gill tissue. Bull. Eur. Ass. Fish Pathol. 19, 149–152.
Torrissen, O.J., Christiansen, R., 1995. Requirements for carotenoids in fish diets. J. Appl. Ichthyol. 11, 225–230.
Urawa, S., 1992. Trichodina truttae Mueller 1937 (Ciliophora, Peritrichida) on juvenile chum salmon (Oncorhynchus
keta)—pathogenicity and host–parasite interactions. Fish Pathol. 27, 29–37.
Urawa, S., 1995. Effects of rearing conditions on growth and mortality of juvenile chum salmon (Oncorhynchus keta)
infected with Icthyobodo necator. Can. J. Fish. Aq. Sci. 52 (Suppl. 1), 18–23.
Uspenskaya, A.V., 1957. The ecology and spreading of the pathogen of trout whirling disease-Myxosoma cerebralis
(Hofer, 1903, Plehn, 1905) in the fish ponds of the Soviet Union, vol. XLII. Izvestiya Vsesoyuznogo naucho-
issledovatel’skogo instituta ozernogo i rechnogo rybnogo khozyaistva.
Wagner, G.N., McKinley, R.S., Bjorn, P.A., Finstad, B., 2004. Short-term freshwater exposure benefits sea lice-infected
Atlantic salmon. J. Fish Biol. 64, 1593–1604.
Ward, A.J.W., Hart, P.J.B., 2003. The effects of kin and familiarity on interactions between fish. Fish Fish 4, 348–358.
Ward, A.J.W., Duff, A.J., Krause, J., Barber, I., 2005. Shoaling behaviour of sticklebacks infected with a microsporidian
parasite. Environ. Biol. Fish. 72, 155–160.
Wertheim, B., Vet, L.E.M., Dicke, M., 2003. Increased risk of parasitism as ecological costs of using aggregation
pheromones: laboratory and field study of Drosophila-Leptopilina interaction. Oikos 100, 269–282.
Williams, H.H., Jones, A., 1994. Parasitic Worms of Fish. Taylor and Francis, London.
Wilson, R.P., 2002. Amino acids and proteins. In: Halver, J.E., Hardy, R.W. (Eds.), Fish Nutrition. third ed. Academic
Press Inc., San Diego, CA, USA, pp. 143–179.
Wright, H.A., Wootton, R.J., Barber, I., 2006. The effect of Schistocephalus solidus infection on meal size of three-spined
stickleback. J. Fish Biol. 68, 801–809.