Variation in emotion and cognition among fishes

Felicity Huntingford & Victoria Braithwaite

University of Glasgow, Glasgow, U.K.Penn State University, PA, U.S.A.

Requested topics• What are the cognitive capacities of fish and do

fish experience emotions?• Are the answers the same for different kinds of

fish? • If not, what are the implications for fish welfare?

• Concepts of cognition and emotion

• Kinds of evidence for cognitive and emotional capacity in non-human animals

• Status of the evidence for fish

• Variability in cognitive and emotional capacity among fish

• Implications for welfare

Issues to address

About definitions of welfare

• To address public concern fully requires consideration of not just the functional responses fish make to challenge but also what they feel

• Nor easy, because ultimately it is impossible to know what a fish (or any non-human animal) feels

• The best we can do is to gather as many sources of indirect evidence as possible about their emotions and cognitive capacities and draw deductions from these.• Hence this meeting?

Emotion and cognition

Emotion: Psychological processes arising when an animal experiences something as positive or rewarding or negative/punishing. Evolved adaptations, enabling animals to gain rewards or desirable resources and to avoid danger and harm. “Adaptive, motivational affective states”Cognition: The processes by which an animal internalises information about past experience and present conditions and adapts subsequent behaviour accordingly. Involves perception, learning and memory

Interpretation of information, which depends on past experience, changes with emotional state, which in turn alters in response to interpreted information

EMOTION PERCEPTION LEARNING & MEMORY

COGNITIVE PROCESSES

COGNITION

Many links between emotion & cognition

Where does welfare come in?

Evidence for cognitive and emotional capacity in non-human animals

Central nervous system: homologous brain machinery to that known to control cognition and emotions in humans?• Neuroanatomy• Neurochemistry

Behaviour (and physiology)

Brain: behaviour links

• Response to negative or positive stimuli• Priorities and choices• Ability to learn• Complexity and flexibility

• Goal directedness• Anticipation

Burns: The capacity to “guess and fear”

Status of fish: neuroanatomy • The lateral and medial pallial regions

of the teleost forebrain are homologous to the mammalian hippocampus and amygdala, which are involved in learning and emotions in mammals, even though they develop in a different way Broglio et al. 2003, 2005.

• Caution is required about using such evidence (either way) based on structure alone: assumes equivalence of function over evolutionary time

Status of fish: neurochemistryDopaminergic and serotoninergic systems in fish

Panula et al 2010

Green = dopaminergic Dark blue = noradrenergic Orange = serotoninergic

Behavioural complexity: status of fish Well developed capacity for learning

Trace Pavlovian conditioning with reinforcer devaluationNordgreen et al. 2009.

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Trace avoidance conditioning Portavella et al 2002.

Complex, flexible behaviour indicative of well developed cognitive capacity

• Groupers and eels

• Reciprocity. Tit-for-tat

• Bystanders and transitive inference

Transitive inference: A>B B>C C>D D>E so B>D etc

Grosenick et al. 2007

What about positive emotions?

• Removal of ectoparasite• Appetance for aggression• Nests and goal directedness

• Self-control/impulse control• Optimal diet choice • Reverse reward contingency

Danisman et al 2010

Complex, flexible behaviour

Status of fish: brain-behaviour links Evidence from lesion experiments that the hippocampus-

and amygdala-equivalents play a role in learning and emotions respectively in fish

Duran et al 2010

Proximal cues removed

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Broglio et al 2005

Summary of forebrain function in fish and mammals

Striking similarity of function

Evidence for role of dopamine in reward and learning in fish

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Matioli et al. 1997

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• Concepts of cognition and emotion• Evidence for cognitive and emotional capacity

in non-human animals• Status of the evidence for fish

• Variability in cognitive and emotional capacity among fish• Implications for welfare

Fish are not mindless robots responding to challenge by simple reflexes with no emotional or cognitive contentThey are capable of complex behaviour indicative of complex cognitive abilitiesStill to make an explicit link between cognitive and emotional status and capacity for suffering or pleasure in fish: work so far necessary but not sufficient

So far:

Variability in emotional and cognitive capacity potentially has implications for welfare

Sources of variability in emotional and cognitive capacity among fishWithin species

• Gender• Life history stage• Life history strategy • Population/strain• Individuals

Between species

Within species: gender

• Dramatic remodelling of brain biochemistry and behaviour when fish change sex

Larson et al 2003

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Days from start of sex change

Bioa

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DAMedial pallium

Female MaleNon territorial Territorial

• Gender differences in emotional (and possibly cognitive) capacities, certainly in adults but even in juveniles

Within species: life history stage

Harvey & Brown 2004

As fish grow, they move through predation windows

% c

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Moving Spines raised Feed latency

With associated changes in risk and response to it

In piscivorous species, above a certain size, prey become predators

Time over year 1

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•Differences in age ofmaturity and mating strategy within cohorts•Striking differences inbehaviour

Kolm et al. 2009

Within species: life history strategy

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Gender and mating strategy

Male FemaleParr Anad Parr Anad

• Differences in relative size of whole brain and cerebellum in male and female trout adopting different mating strategies

Within species: individual stress coping styles

Adrenaline

Noradrenaline

Dopamine

Adrenaline Brelin et al. 2008

• Two kinds of wild brown trout• Differ in risk-taking and aggression• And in stress physiology• “Proactive” and “reactive”

• Different proportions of proactive and reactive fish in laboratory-reared trout from large, stocked river and small, unstocked streams.

Within species: populations

% p

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fish

Brelin et al. 2008

• Associated with differences in response to hypoxia

100-70 50 30 20 Oxygen saturation (%)

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Within species: population differences in learning

Braithwaite & Girvan 2003

Sticklebacks from river and pond populations given the opportunity to find food using visual landmarks or direction of water flow

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• River fish use flow• Pond fish use landmarks

• Because of indeterminate growth rates and flexible sex determination (among other things), in fish more than in other vertebrates there is much variation in behaviour, physiology and brain function within a species.

• This is relevant to welfare, generating different responses to important challenges, with associated differences in mortality risk .

So far:

Between species: emotion and cognition

Differences in learning: 3 spined sticklebacks, but not 9 spined sticklebacks, alter their behaviour in response to paternal chases

Response to predation risk: 3 and 9 spined sticklebacks. Differences in response to risk (fear) in many contexts related to relative predation risk.

Even among closely related teleosts, emotional responses and cognitive capacities are variable, in relation to ecological factors.

Between species: overall brain size

• Striking variability in overall brain size. • Largely due to body size• But not entirely

Sharks

Teleosts

Pelagic fish

Linsey & Collin 2006

Between species: specific brains regions

And in rates of evolution of different brain regions (Tanganyikan cichlids)

Olfactory bulbTelencephalon

Gonzales-Voyer et al 2006

Difference in relative size of brain regions North American shiners %

var

iabi

lity

Kotreschal et al. 1998

Partly related to taxonomy

Ray finned fish

Lobe finned fish

Partly related to ecology

Trophic status

• Cichlids that feed on sessile food items have larger brains than those feeding on motile prey. Gonzalez-Voyer et al. 2009

• In fish generally, prey species have larger brains that do their associated predators

• Larger-brained predators tend to hunt larger-brained prey.

• Complicated relationship between trophic level and brain size Kondoh 2009.

Brain/body size prey

Bra

in/b

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size

pre

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Social organisation

Pollen et al. 2007 Stumway 2008

• In Tanganyka cichlids, the telencephalon tends to be larger in mongamous than polygamous species. • Monogamous species have greater visual acuity, but fewer social interactions.

Habitat complexity is associated with a larger cerebellum (more complex movement) and telencephalon (additional computational capacity) Pollen et al. 2007

Habitat complexity

Telencephalon

RockSand

Cerebellum

RockSand

Rock dwelling species have a relatively larger telecephalon and cerebellum, better visual acuity and better ability to use spatial cues to find food.

Shumway 2008a

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Some conclusions • Not clear how much of this variability represents inherited adaptation and how much is the effect of plasticity in brain growth. • Level of analysis is still very crude.• Size is not everything.

• All the same, comparative studies of brain, ecology and behaviour throw light on the selective forces that shape the evolution of brain structure and of cognitive ability. • Evolutionary biologists can (are starting to be able to) predict from taxonomy, habitat, diet and social organisation how complex a fish’s brain and behaviour are likely to be.

So what? Implications of this variability for welfare

Linking welfare to cognition and emotion Welfare scientists can use variability in emotion, cognition

and underlying brain machinery in fish (both between and within species) to probe the difficult relationship between behavioural complexity, brain structure and welfare.

EMOTION PERCEPTION LEARNING & MEMORY

COGNITIVE PROCESSES

COGNITION

Where does welfare come in?

• The is no “one size fits all” answer to the general question of whether fish can suffer of feel pleasure. This will depend in any given case on the general cognitive and emotional capacity of the species (and life history stage etc) concerned.

Implications of this variability for welfare: Can fish suffer and enjoy?

• Nor is there a single answer to the specific question of what circumstances will cause a given species of fish suffering or pleasure. This will depend on specific cognitive and emotional systems of the species (and life history stage etc) concerned.

• Does what is known about variable emotional and cognitive capacities in fish help in drawing a line between animals whose welfare does and does not matter?

Almost certainly not, partly because a clear line probably does not exist and partly because we do not have sufficiently precise tools to locate it (yet?). But fish might be ranked by susceptibility to poor welfare

• Could we perhaps get to the point of having “look up” tables for which species, strain or life history stage and life history strategy to use for any given purpose to minimise suffering?

Almost certainly not, but thinking about this might help to identify the important gaps in knowledge

Choosing subjects for welfare-friendly exploitation?