Variation in emotion and cognition among fishes Felicity Huntingford & Victoria Braithwaite

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

7. 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” 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

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. No shock Shock Training Devaluation Trace avoidance conditioning Portavella et al 2002. Behavioural complexity: status of fish Well developed capacity for learning • Trace Pavlovian conditioning with reinforcer devaluation • Nordgreen et al. 2009.

11. 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 Complex, flexible behaviour indicative of well developed cognitive capacity

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

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. SP (dopamine) mediation of discrimination learning Reinforcing effects of SP (dopamine) administration Unpaired Paired Train Test Rev1 Rev2 Rev3 Rev4 Control SP25 SP50 SP50 +DAant Matioli et al. 1997 Matioli et al. 1993 Evidence for role of dopamine in reward and learning in fish

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

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

19. In piscivorous species, above a certain size, prey become predators With associated changes in risk and response to it Within species: life history stage As fish grow, they move through predation windows Percentage in diet Time over year 1 % change from control Moving Spines raised Feed latency 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 Kolm et al. 2009

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

22. Associated with differences in response to hypoxia Within species: populations Escape attempts/min • Different proportions of proactive and reactive fish in laboratory-reared trout from large, stocked river and small, unstocked streams. % proactive fish 100-70 50 30 20 Oxygen saturation (%) Brelin et al. 2008

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

26. Teleosts Pelagic fish Sharks Between species: overall brain size • Striking variability in • overall brain size. • Largely due to body size • But not entirely Linsey & Collin 2006

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

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

29. 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. 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 Brain/body size predator Brain/body size prey

30. In Tanganyka cichlids, the telencephalon tends to be larger in mongamous than polygamous species. • Monogamous species have greater visual acuity, but fewer social interactions. Social organisation 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 Telencephalon Cerebellum Rock Sand 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 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. Where does welfare come in? LEARNING & MEMORY PERCEPTION EMOTION 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. COGNITIVE PROCESSES COGNITION

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