Animal Cognition

, Volume 15, Issue 5, pp 903–911 | Cite as

Omission of expected reward agitates Atlantic salmon (Salmo salar)

  • Marco A. Vindas
  • Ole Folkedal
  • Tore S. Kristiansen
  • Lars H. Stien
  • Bjarne O. Braastad
  • Ian Mayer
  • Øyvind Øverli
Original Paper


The evolutionary background for cognition and awareness is currently under ardent scrutiny. Poikilothermic vertebrates such as teleost fishes are capable of classical conditioning and have long-term memories, but it remains unknown to what degree such capabilities are associated with affective states. Here, we investigate whether the concept of frustration may apply to Atlantic salmon. In mammals, this paradigm comprises the omission of an expected reward (OER), which elicits behavioural and physiological coping responses (e.g. aggression and stress reactions). Six groups with 200 fish in each were conditioned to associate a flashing light (CS) with feeding. Conditioning over 22 days led to a change from aversion to attraction to the CS. Subsequently, 3 groups served as control, and 3 groups were subjected to an OER paradigm for 9 days, in which the expected food reward was delayed for 30 min during two out of three daily meals. Compared to controls, OER groups displayed higher levels of aggression and more heterogeneous growth rates, indicating a more pronounced social hierarchy. Cortisol levels did, however, not differ between treatments and both groups responded similarly to acute stress. These results indicate that teleost fishes, like mammals, respond aggressively to OER. The capacity to respond behaviourally to frustrating conditions thus likely reflects an adaptive response to environmental unpredictability, which has been conserved throughout vertebrate evolution.


Frustration Aggression Classical conditioning Stress Cognition Animal welfare 


  1. Amsel A (1958) The role of frustrative nonreward in noncontinuous reward situations. Psychol Bull 55:102–119PubMedCrossRefGoogle Scholar
  2. Amsel A (1992) Frustration theory: many years later. Psychol Bull 112:396–399PubMedCrossRefGoogle Scholar
  3. Bratland S, Stien L, Braithwaite VA, Juell J-E, Folkedal O, Nilsson J, Oppedal F, Fosseidengen J, Kristiansen TS (2010) From fright to anticipation: using aversive light stimuli to investigate reward conditioning in large groups of Atlantic salmon (Salmo salar). Aquacult Int 18:991–1001CrossRefGoogle Scholar
  4. Broglio C, Gómez A, Durán E, Salas C, Rodríguez F (2011) Brain and cognition in teleost fish. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Oxford, pp 325–358CrossRefGoogle Scholar
  5. Brown C, Laland KN (2002) Social learning of a novel avoidance task in the guppy: conformity and social release. Anim Behav 64:41–47CrossRefGoogle Scholar
  6. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288CrossRefGoogle Scholar
  7. Brown G, Ferrari MCO, Chivers DP (2011) Learning about danger: chemical alarm cues and threat-sensitive assessment of predation risk by fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Oxford, pp 59–80CrossRefGoogle Scholar
  8. Carlstead K (1986) Predictability of feeding: its effect on agonistic behaviour and growth in grower pigs. Appl Anim Behav Sci 16:25–38CrossRefGoogle Scholar
  9. Dantzer R, Arnone M, Mormede P (1980) Effects of frustration on behaviour and plasma corticosteroid levels in pigs. Physiol Behav 24:1–4PubMedCrossRefGoogle Scholar
  10. Duncan IJH, Wood-Gush DGM (1971) Frustration and aggression in the domestic fowl. Anim Behav 19:500–504PubMedCrossRefGoogle Scholar
  11. Einum S, Fleming IA (1997) Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J Fish Biol 50:634–651CrossRefGoogle Scholar
  12. Fernö A, Huse G, Jakobsen PJ, Kristiansen TS, Nilsson J (2011) Fish behaviour, learning aquaculture and fisheries. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Oxford, pp 359–404CrossRefGoogle Scholar
  13. Ferrari MCO, Brown GE, Bortolotti GR, Chivers DP (2010) Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles. Proc R Soc 277B:2205–2210Google Scholar
  14. Folkedal O, Stien LH, Torgersen T, Oppedal F, Olsen RE, Fosseidengen JE, Braithwaite VA, Kristiansen TS (2012a) Food anticipatory behaviour as an indicator of stress response and recovery in Atlantic salmon post-smolt after exposure to acute temperature fluctuation. Physiol Behav 105:350–356PubMedCrossRefGoogle Scholar
  15. Folkedal O, Torgersen T, Olsen RE, Fernö A, Nilsson J, Oppedal F, Stien LH, Kristiansen TS (2012b) Duration of effects of acute environmental changes on food anticipatory behaviour, feed intake, oxygen consumption, and cortisol release in Atlantic salmon parr. Physiol Behav 105:283–291PubMedCrossRefGoogle Scholar
  16. Gonzalez RC, Holmes NK, Bitterman ME (1967) Resistance to extinction in the goldfish as a function of frequency and amount of reward. Am J Psychol 80:269–275PubMedCrossRefGoogle Scholar
  17. Huntingford FA, Adams C, Braithwaite VA, Kadri S, Pottinger TG, Sandøe P, Turnbull JF (2006) Current issues in fish welfare. J Fish Biol 68:332–372CrossRefGoogle Scholar
  18. Janhunen M, Peuhkuri N, Piironen J (2010) A comparison of growth patterns between a stunted and two large predatory Arctic charr populations under identical hatchery conditions. Env Biol Fish 87:113–121CrossRefGoogle Scholar
  19. Jobling M (1995) Simple indices for the assessment of the influences of social environment on growth performance, exemplified by studies on Arctic charr. Aquacult Int 3:60–65Google Scholar
  20. Jørgensen EH, Christiansen JS, Jobling M (1993) Effects of stocking density on food intake, growth performance and oxygen consumption in Arctic charr (Salvelinus alpinus). Aquaculture 110:191–204CrossRefGoogle Scholar
  21. Keenleyside MHA, Yamamoto FT (1962) Territorial behaviour of juvenile Atlantic salmon (Salmo salar L.). Behaviour 19:139–169CrossRefGoogle Scholar
  22. Laland K, Brown C, Krause J (2003) Learning in fishes: from three-second memory to culture. Fish Fish 4:199–202CrossRefGoogle Scholar
  23. Lindeyer CM, Reader SM (2010) Social learning of escape routes in zebrafish and the stability of behavioural traditions. Anim Behav 79:827–834CrossRefGoogle Scholar
  24. Mackintosh NJ (1971) Reward and aftereffects of reward in the learning of goldfish. J Comp Physiol Psychol 76:225–232PubMedCrossRefGoogle Scholar
  25. Marcus-Newhall A, Pedersen WC, Carlson M, Miller N (2000) Displaced aggression is alive and well: a meta-analytic review. J Pers Soc Psychol 78:670–689PubMedCrossRefGoogle Scholar
  26. Martins C, Galhardo L, Noble C, Damsgård B, Spedicato M, Zupa W, Beauchaud M, Kulczykowska E, Massabuau J-C, Carter T, Planellas S, Kristiansen T (2012) Behavioural indicators of welfare in farmed fish. Fish Physiol Biochem 38:17–41PubMedCrossRefGoogle Scholar
  27. Mayer I, Lundqvist H, Berglund I, Schmitz M, Schulz R, Borg B (1990) Seasonal endocrine changes in Baltic salmon (Salmo salar), immature parr and mature male parr. I. Plasma levels of five androgens, 17α-hydroxy-20β-dihydroprogesterone, and 17β-estradiol. Can J Zool 68:1360–1365CrossRefGoogle Scholar
  28. Nilsson J, Kristiansen TS, Fosseidengen J, Fernö A, van den Bos R (2008a) Learning in cod (Gadus morhua): long trace interval retention. Anim Cogn 11:215–222PubMedCrossRefGoogle Scholar
  29. Nilsson J, Kristiansen TS, Fosseidengen J, Fernö A, van den Bos R (2008b) Sign- and goal-tracking in Atlantic cod (Gadus morhua). Anim Cogn 11:651–659PubMedCrossRefGoogle Scholar
  30. Nilsson J, Kristiansen TS, Fosseidengen JE, Stien LH, Fernö A, van den Bos R (2010) Learning and anticipatory behaviour in a “sit-and-wait” predator: The Atlantic halibut. Behav Process 83:257–266CrossRefGoogle Scholar
  31. Nordgreen J, Janczak A, Hovland A, Ranheim B, Horsberg T (2010) Trace classical conditioning in rainbow trout (Oncorhynchus mykiss): what do they learn? Anim Cogn 13:303–309PubMedCrossRefGoogle Scholar
  32. Øverli Ø, Harris CA, Winberg S (1999) Short-term effects of fights for social dominance and the establishment of dominant-subordinate relationships on brain monoamines and cortisol in rainbow trout. Brain Behav Evol 54:263–275PubMedCrossRefGoogle Scholar
  33. Øverli Ø, Korzan WJ, Larson ET, Winberg S, Lepage O, Pottinger TG, Renner KJ, Summers CH (2004) Behavioural and neuroendocrine correlates of displaced aggression in trout. Horm Behav 45(5):324–329PubMedCrossRefGoogle Scholar
  34. Øverli Ø, Sørensen C, Pulman KGT, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007) Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412PubMedCrossRefGoogle Scholar
  35. Papini MR (2003) Comparative psychology of surprising nonreward. Brain Behav Evol 62:83–95PubMedCrossRefGoogle Scholar
  36. Papini MR, Dudley RT (1997) Consequences of surprising reward omissions. Rev Gen Psychol 1:175–197CrossRefGoogle Scholar
  37. Papini MR, Muzio RN, Segura ET (1995) Instrumental learning in toads (Bufo arenarum): reinforcer magnitude and the medial pallium. Brain Behav Evol 46:61–71PubMedCrossRefGoogle Scholar
  38. Portavella M, Vargas JP, Torres B, Salas C (2002) The effects of telencephalic pallial lesions on spatial, temporal, and emotional learning in goldfish. Brain Res Bull 57:397–399PubMedCrossRefGoogle Scholar
  39. Portavella M, Torres B, Salas C (2004) Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24:2335–2342PubMedCrossRefGoogle Scholar
  40. Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol tesponse to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132PubMedCrossRefGoogle Scholar
  41. Sapolsky RM (2004) Why zebras don’t get ulcers. Henry Holt and Company (Holt paperbacks), New YorkGoogle Scholar
  42. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27PubMedGoogle Scholar
  43. Thomassen JM, Fjæra SO (1991) Use of light signalling before feeding of salmon (Salmo salar). Aquacult Eng 10:65–71CrossRefGoogle Scholar
  44. Warburton K, Hughes R (2011) Learning of foraging skills by fish. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Oxford, pp 10–35CrossRefGoogle Scholar
  45. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625PubMedGoogle Scholar
  46. Winberg S, Nilsson GE (1993) Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp Biochem Physiol 106C:597–614Google Scholar
  47. Winberg S, Nilsson GE, Olsén KH (1992) Changes in brain serotonergic activity during hierarchic behavior in Arctic charr (Salvelinus alpinus L.) are socially induced. J Comp Physiol 170A:93–99Google Scholar
  48. Winberg S, Carter CG, Mccarthy ID, He ZY, Nilsson GE, Houlihan DF (1993) Feeding rank and brain serotonergic activity in rainbow trout Oncorhyncus mykiss. J Exp Biol 179:197–211Google Scholar
  49. Zimmerman PH, Koene P (1998) The effect of frustrative nonreward on vocalisations and behaviour in the laying hen, Gallus gallus domesticus. Behav Process 44:73–79CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Marco A. Vindas
    • 1
  • Ole Folkedal
    • 2
  • Tore S. Kristiansen
    • 2
  • Lars H. Stien
    • 2
  • Bjarne O. Braastad
    • 1
  • Ian Mayer
    • 3
  • Øyvind Øverli
    • 1
  1. 1.Norwegian University of Life SciencesÅsNorway
  2. 2.Institute of Marine ResearchStorebøNorway
  3. 3.The Norwegian School of Veterinary ScienceOsloNorway

Personalised recommendations