1. University of Glasgow, Glasgow, U.K. Penn State University, PA, U.S.A.
Variation in emotion and cognition among fishes Felicity Huntingford & Victoria Braithwaite
University of Glasgow, Glasgow, U.K.
Penn State University, PA, U.S.A.

2. 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?

3. Issues to address 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

4. 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?

5. 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

6. Where does welfare come in?
Many links between emotion & cognition
EMOTION
PERCEPTION
LEARNING & MEMORY
COGNITIVE PROCESSES
COGNITION
Where does welfare come in?
Interpretation of information, which depends on past experience, changes with emotional state, which in turn alters in response to interpreted information

7. 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)
Response to negative or positive stimuli
Priorities and choices
Ability to learn
Complexity and flexibility
Goal directedness
Anticipation
To a Mouse. (last verse)
Robert Burns To a mouse.
  “Still thou are blest compared wi’ me!
The present only touches thee;
But, Och! I backwards cast my e’e on prospects drear!
An’ forward, tho’ I cannot see, I guess an’ fear!”
Burns: The capacity to “guess and fear”
Brain: behaviour links

8. 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

9. Status of fish: neurochemistry
Dopaminergic and serotoninergic systems in fish
Green = dopaminergic
Dark blue = noradrenergic
Orange = serotoninergic
Panula et al 2010

10. Behavioural complexity: status of fish
Well developed capacity for learning
Trace Pavlovian conditioning with reinforcer devaluation
Nordgreen et al
Training Devaluation
No shock
Shock
Trace avoidance conditioning
Portavella et al 2002.

11. Complex, flexible behaviour
indicative of well developed cognitive capacity
Bystanders and transitive inference
Transitive inference:
A>B B>C C>D D>E so B>D etc
Grosenick et al. 2007
Reciprocity. Tit-for-tat
Groupers and eels

12. What about positive emotions?
Danisman et al 2010
Complex, flexible behaviour
Self-control/impulse control
Optimal diet choice
Reverse reward
contingency
What about positive emotions?
Removal of ectoparasite
Appetance for aggression
Nests and goal directedness

13. 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

14. Summary of forebrain function
in fish and mammals
Broglio et al 2005
Striking similarity of function

15. Evidence for role of dopamine in reward and learning in fish
Control SP SP SP50
+DAant
Unpaired
Paired
Matioli et al. 1993
Reinforcing effects of SP (dopamine) administration
Matioli et al. 1997
Train Test Rev1 Rev2 Rev3 Rev4
SP (dopamine) mediation of discrimination learning

16. So far: Variability in cognitive and emotional capacity among fish
Concepts of cognition and emotion
Evidence for cognitive and emotional capacity in non-human animals
Status of the evidence for fish
Fish are not mindless robots responding to challenge by simple reflexes with no emotional or cognitive content
They are capable of complex behaviour indicative of complex cognitive abilities
Still 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
Variability in cognitive and emotional capacity among fish
Implications for welfare

17. Sources of variability in emotional and cognitive capacity among fish
Between species
Within species
Gender
Life history stage
Life history strategy
Population/strain
Individuals
Variability in emotional and cognitive capacity potentially has implications for welfare

18. Within species: gender
Gender differences in emotional (and possibly cognitive) capacities, certainly in adults but even in juveniles
Dramatic remodelling of brain biochemistry and behaviour when fish change sex
Larson et al 2003
Medial pallium
Female Male
Non territorial Territorial
SEs still to be added

19. Within species: life history stage
In piscivorous species,
above a certain size, prey
become predators
Time over year 1
Percentage in diet
As fish grow, they move
through predation windows
% change from control
Moving Spines raised Feed latency
With associated changes in risk and response to it
Figure still to come if decide to include
Harvey & Brown 2004

20. Within species: life history strategy
Male Female
Parr Anad Parr Anad
Differences in relative size
of whole brain and
cerebellum in male and
female trout adopting
different mating strategies
Differences in age of
maturity and mating
strategy within cohorts
Striking differences in
behaviour
SEs and legends to be added if decide to use.
Kolm et al. 2009

21. individual stress coping styles
Within species:
individual stress coping styles
Adrenaline
Noradrenaline
Dopamine
Brelin et al. 2008
Two kinds of wild brown trout
Differ in risk-taking and aggression
And in stress physiology
“Proactive” and “reactive”
Redraw and sim
plify figs

22. Within species: populations
Different proportions of proactive and reactive fish in laboratory-reared trout from large, stocked river and small, unstocked streams.
% proactive fish
Associated with
differences in response
to hypoxia
Oxygen saturation (%)
Escape attempts/min
Brelin et al. 2008

23. Within species: population differences in learning
Sticklebacks from river and pond populations given the opportunity to find food using visual landmarks or direction of water flow
Percentage of fish
River fish use flow
Pond fish use
landmarks
Braithwaite & Girvan 2003

24. So far:
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 .

25. Between species: emotion and cognition
Response to predation risk: 3 and 9 spined sticklebacks. Differences in response to risk (fear) in many contexts related to relative predation risk.
Between species:
emotion and cognition
Differences in learning: 3 spined sticklebacks, but not 9 spined sticklebacks, alter their behaviour in response to paternal chases
Even among closely related teleosts, emotional responses and cognitive capacities are variable, in relation to ecological factors.

26. Between species: overall brain size Striking variability in
Sharks
Teleosts
Pelagic fish
Striking variability in
overall brain size.
Largely due to body size
But not entirely
These are still notes to myself. Will simplify
Redraw and simplify figs
Linsey & Collin 2006

27. specific brains regions
Between species:
specific brains regions
Difference in relative size of brain regions
North American shiners
% variability
Kotreschal et al. 1998
And in rates of evolution of different brain regions (Tanganyikan cichlids)
Olfactory bulb
Telencephalon
Gonzales-Voyer et al 2006

28. Partly related to taxonomy
Ray finned fish
Lobe finned fish

29. 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
Brain/body size predator

30. Social organisation
In Tanganyka cichlids, the telencephalon tends to be larger in mongamous than polygamous species.
Monogamous species have greater visual acuity, but fewer social interactions.
These are still notes to myself. Will simplify
Pollen et al. 2007
Stumway 2008

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

32. Rock dwelling species have a relatively larger telecephalon and cerebellum, better visual acuity and better ability to use spatial cues to find food.
Telen
Cereb
Midbr
Hypoth
Brain
Medulla
Olf bulb
Redraw figures
Landmark
Shumway 2008a

33. 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.

34. 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?
Thinking aloud here

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

36. Choosing subjects for welfare-friendly exploitation?
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?
Still thinking aloud. Working on this
Almost certainly not, but thinking about this might help to identify the important gaps in knowledge