parasites, behaviour and welfare in fish

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

www.elsevier.com/locate/applanim

Applied Animal Behaviour Science 104 (2007) 251–264

* 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: [email protected].

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.applanim.2006.09.005

mailto:[email protected]

http://dx.doi.org/10.1016/j.applanim.2006.09.005

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) 251–264252

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

I. Barber / Applied Animal Behaviour Science 104 (2007) 251–264 253

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].

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


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 Cote 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


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.


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


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 (Seppala 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


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 (Ostlund-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


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


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.

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