Abstract
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.
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References
Amsel A (1958) The role of frustrative nonreward in noncontinuous reward situations. Psychol Bull 55:102–119
Amsel A (1992) Frustration theory: many years later. Psychol Bull 112:396–399
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 18:991–1001
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 325–358
Brown C, Laland KN (2002) Social learning of a novel avoidance task in the guppy: conformity and social release. Anim Behav 64:41–47
Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288
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 59–80
Carlstead K (1986) Predictability of feeding: its effect on agonistic behaviour and growth in grower pigs. Appl Anim Behav Sci 16:25–38
Dantzer R, Arnone M, Mormede P (1980) Effects of frustration on behaviour and plasma corticosteroid levels in pigs. Physiol Behav 24:1–4
Duncan IJH, Wood-Gush DGM (1971) Frustration and aggression in the domestic fowl. Anim Behav 19:500–504
Einum S, Fleming IA (1997) Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J Fish Biol 50:634–651
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 359–404
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:2205–2210
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 105:350–356
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 105:283–291
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 80:269–275
Huntingford FA, Adams C, Braithwaite VA, Kadri S, Pottinger TG, Sandøe P, Turnbull JF (2006) Current issues in fish welfare. J Fish Biol 68:332–372
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 87:113–121
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 3:60–65
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 110:191–204
Keenleyside MHA, Yamamoto FT (1962) Territorial behaviour of juvenile Atlantic salmon (Salmo salar L.). Behaviour 19:139–169
Laland K, Brown C, Krause J (2003) Learning in fishes: from three-second memory to culture. Fish Fish 4:199–202
Lindeyer CM, Reader SM (2010) Social learning of escape routes in zebrafish and the stability of behavioural traditions. Anim Behav 79:827–834
Mackintosh NJ (1971) Reward and aftereffects of reward in the learning of goldfish. J Comp Physiol Psychol 76:225–232
Marcus-Newhall A, Pedersen WC, Carlson M, Miller N (2000) Displaced aggression is alive and well: a meta-analytic review. J Pers Soc Psychol 78:670–689
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 38:17–41
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 68:1360–1365
Nilsson J, Kristiansen TS, Fosseidengen J, Fernö A, van den Bos R (2008a) Learning in cod (Gadus morhua): long trace interval retention. Anim Cogn 11:215–222
Nilsson J, Kristiansen TS, Fosseidengen J, Fernö A, van den Bos R (2008b) Sign- and goal-tracking in Atlantic cod (Gadus morhua). Anim Cogn 11:651–659
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 83:257–266
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 13:303–309
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 54:263–275
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):324–329
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 31:396–412
Papini MR (2003) Comparative psychology of surprising nonreward. Brain Behav Evol 62:83–95
Papini MR, Dudley RT (1997) Consequences of surprising reward omissions. Rev Gen Psychol 1:175–197
Papini MR, Muzio RN, Segura ET (1995) Instrumental learning in toads (Bufo arenarum): reinforcer magnitude and the medial pallium. Brain Behav Evol 46:61–71
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 57:397–399
Portavella M, Torres B, Salas C (2004) Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24:2335–2342
Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol tesponse to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132
Sapolsky RM (2004) Why zebras don’t get ulcers. Henry Holt and Company (Holt paperbacks), New York
Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27
Thomassen JM, Fjæra SO (1991) Use of light signalling before feeding of salmon (Salmo salar). Aquacult Eng 10:65–71
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 10–35
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625
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:597–614
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:93–99
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 179:197–211
Zimmerman PH, Koene P (1998) The effect of frustrative nonreward on vocalisations and behaviour in the laying hen, Gallus gallus domesticus. Behav Process 44:73–79
Acknowledgments
This study has been carried out with financial support from the Research Council of Norway, Project 119728 SALMOWA (www.imr.no/salmowa/). We are grateful to the staff of the Matre Aquaculture Research Station for their technical assistance and two anonymous referees for comments that improved the manuscript.
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Vindas, M.A., Folkedal, O., Kristiansen, T.S. et al. Omission of expected reward agitates Atlantic salmon (Salmo salar). Anim Cogn 15, 903–911 (2012). https://doi.org/10.1007/s10071-012-0517-7
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DOI: https://doi.org/10.1007/s10071-012-0517-7