Switch from fight-flight to freeze-hide: The impacts of severe stress and brain serotonin on behavioral adaptations in flatfish.
5-HT receptor subtype 1A
Behavior
Coping style
Metabolic rate
Serotonin
Stress
Journal
Fish physiology and biochemistry
ISSN: 1573-5168
Titre abrégé: Fish Physiol Biochem
Pays: Netherlands
ID NLM: 100955049
Informations de publication
Date de publication:
03 Feb 2024
03 Feb 2024
Historique:
received:
05
06
2023
accepted:
01
01
2024
medline:
3
2
2024
pubmed:
3
2
2024
entrez:
3
2
2024
Statut:
aheadofprint
Résumé
Animals often experience changes in their environment that can be perceived as stressful. Previous evidence indicates that different individuals may have distinct stress responses. The role of serotonin (5-HT) in stress adaptation is well established, but its relationship with different defense strategies and the persistence of physiological and behavioral responses in different individuals during repeated acute stress remain unclear. In this study, using olive flounder (Paralichthys olivaceus) as a model, we analyzed the relationship between boldness and neurotransmitter 5-HT activity. We found that 5-HT suppression with 5-HT synthesis inhibitor p-chlorophenylalanine (pCPA) and 5-HT receptor subtype 1A (5-HT
Identifiants
pubmed: 38308734
doi: 10.1007/s10695-024-01298-6
pii: 10.1007/s10695-024-01298-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 32273103
Organisme : National Natural Science Foundation of China
ID : 32273103
Organisme : National Natural Science Foundation of China
ID : 32273103
Organisme : National Natural Science Foundation of China
ID : 32273103
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Adams CF, Liley NR, Gorzalka BB (1996) PCPA increases aggression in male firemouth cichlids. Pharmacology 53:328–330. https://doi.org/10.1159/000139446
doi: 10.1159/000139446
pubmed: 8990492
Alfonso S, Sadoul B, Cousin X, Bégout M-L (2020) Spatial distribution and activity patterns as welfare indicators in response to water quality changes in European sea bass, Dicentrarchus labrax. Appl Anim Behav Sci 226:104974. https://doi.org/10.1016/j.applanim.2020.104974
Alfonso S, Sadoul B, Gesto M, Joassard L, Chatain B et al (2019) Coping styles in European sea bass: The link between boldness, stress response and neurogenesis. Physiol Behav 207:76–85. https://doi.org/10.1016/j.physbeh.2019.04.020
doi: 10.1016/j.physbeh.2019.04.020
pubmed: 31047951
Beulig A, Fowler J (2008) Fish on Prozac: Effect of serotonin reuptake inhibitors on cognition in goldfish. Behav Neurosci 122:426–432. https://doi.org/10.1037/0735-7044.122.2.426
doi: 10.1037/0735-7044.122.2.426
pubmed: 18410181
Brierley MJ, Ashworth AJ, Banks JR, Balment RJ, McCrohan CR (2001) Bursting properties of caudal neurosecretory cells in the flounder Platichthys flesus, in vitro. J Exp Biol 204:2733–2739. https://doi.org/10.1242/jeb.204.15.2733
doi: 10.1242/jeb.204.15.2733
pubmed: 11533123
Brierley MJ, Ashworth AJ, Craven TP, Woodburn M, Banks JR et al (2003) Electrical activity of caudal neurosecretory neurons in seawater- and freshwater-adapted flounder: Responses to cholinergic agonists. J Exp Biol 206:4011–4020. https://doi.org/10.1242/jeb.00631
doi: 10.1242/jeb.00631
pubmed: 14555741
Brierley MJ, Bauer CS, Lu W, Riccardi D, Balment RJ et al (2004) Voltage- and Ca2+-dependent burst generation in neuroendocrine dahlgren cells in the teleost Platichthys flesus. J Neuroendocrinol 16:832–841. https://doi.org/10.1111/j.1365-2826.2004.01238.x
doi: 10.1111/j.1365-2826.2004.01238.x
pubmed: 15500543
Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: Consequences of an energetic definition of fitness. Am Nat 142:573–584. https://doi.org/10.1086/285558
doi: 10.1086/285558
pubmed: 19425961
Buchanan CP, Shrier EM, Hill WL (1994) Time-dependent effects of PCPA on social aggression in chicks. Pharmacol Biochem Behav 49:483–488. https://doi.org/10.1016/0091-3057(94)90059-0
doi: 10.1016/0091-3057(94)90059-0
pubmed: 7862698
Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: What are behavioural ecologists measuring? Biol Rev 88:465–475. https://doi.org/10.1111/brv.12007
doi: 10.1111/brv.12007
pubmed: 23253069
Castanheira MF, Conceiçao LEC, Millot S, Rey S, Bégout ML et al (2015) Coping styles in farmed fish: Consequences for aquaculture. Rev Aquac 9:23–41. https://doi.org/10.1111/raq.12100
doi: 10.1111/raq.12100
Castanheira MF, Herrera M, Costas B, Conceição LEC, Martins CIM (2013) Can we predict personality in fish? Searching for consistency over time and across contexts. PLoS One 8:e62037. https://doi.org/10.1371/journal.pone.0062037
doi: 10.1371/journal.pone.0062037
pubmed: 23614007
pmcid: 3628343
Clements S, Moore FL, Schreck CB (2003) Evidence that acute serotonergic activation potentiates the locomotor-stimulating effects of corticotropin-releasing hormone in juvenile Chinook salmon (Oncorhynchus tshawytscha). Horm Behav 43:214–221. https://doi.org/10.1016/S0018-506X(02)00027-2
doi: 10.1016/S0018-506X(02)00027-2
pubmed: 12614652
Clotfelter ED, P. O’Hare E, McNitt MM, Carpenter RE, Summers CH (2007) Serotonin decreases aggression via 5-HT
Cooke SJ, Messmer V, Tobin AJ, Pratchett MS, Clark TD (2014) Refuge-seeking impairments mirror metabolic recovery following fisheries-related stressors in the Spanish flag snapper (Lutjanus carponotatus) on the Great Barrier Reef. Physiol Biochem Zool 87:136–147. https://doi.org/10.1086/671166
doi: 10.1086/671166
pubmed: 24457928
Dahlbom SJ, Backstrom T, Lundstedt-Enkel K, Winberg S (2012a) Aggression and monoamines: Effects of sex and social rank in zebrafish (Danio rerio). Behav Brain Res 228:333–338. https://doi.org/10.1016/j.bbr.2011.12.011
doi: 10.1016/j.bbr.2011.12.011
pubmed: 22192379
Dahlbom SJ, Backström T, Lundstedt-Enkel K, Winberg S (2012b) Aggression and monoamines: effects of sex and social rank in zebrafish (Danio rerio). Behav Brain Res 228:333–338. https://doi.org/10.1016/j.bbr.2011.12.011
doi: 10.1016/j.bbr.2011.12.011
pubmed: 22192379
Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: Consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739. https://doi.org/10.1111/j.1461-0248.2004.00618.x
doi: 10.1111/j.1461-0248.2004.00618.x
Dochtermann NA (2010) Behavioral syndromes: Carryover effects, false discovery rates, and a priori hypotheses. Behav Ecol 21:437–439. https://doi.org/10.1093/beheco/arq021
doi: 10.1093/beheco/arq021
Dray S, Dufour A, Thioulouse, Jean, Pavoine S et al (2015) Ade4: analysis of ecological data: Exploratory and Euclidean methods in environmental sciences. http://CRAN.Rproject.org/package=ade4
Edwards DH, Kravitz EA (1997) Serotonin, social status and aggression. Curr Opin Neurobiol 7:812–819. https://doi.org/10.1016/S0959-4388(97)80140-7
doi: 10.1016/S0959-4388(97)80140-7
pubmed: 9464985
Ferguson RA, Tufts BL (1992) Physiological effects of brief air exposure in exhaustively exercised rainbow trout (Oncorhynchus mykiss): implications for “catch and release” fisheries. Can J Fish Aquat Sci 49:1157–1162. https://doi.org/10.1139/f92-129
doi: 10.1139/f92-129
Fillion G (1983) 5-Hydroxytryptamine receptors in brain. Springer, Boston
doi: 10.1007/978-1-4684-4361-5_4
Gesto M, Lopez-Patino MA, Hernandez J, Soengas JL, Miguez JM (2013) The response of brain serotonergic and dopaminergic systems to an acute stressor in rainbow trout: A time course study. J Exp Biol 216:4435–4442. https://doi.org/10.1242/jeb.091751
doi: 10.1242/jeb.091751
pubmed: 24031060
Glimcher PW, Rustichini A (2004) Neuroeconomics: The consilience of brain and decision. Science 306:447–452. https://doi.org/10.1126/science.1102566
doi: 10.1126/science.1102566
pubmed: 15486291
Höglund E, Bakke MJ, Øverli Ø, Winberg S, Nilsson GE (2005) Suppression of aggressive behaviour in juvenile Atlantic cod (Gadus morhua) by L-tryptophan supplementation. Aquaculture 249:525–531. https://doi.org/10.1016/j.aquaculture.2005.04.028
doi: 10.1016/j.aquaculture.2005.04.028
Höglund E, Balm PHM, Winberg S (2000) Skin darkening, a potential social signal in subordinate Arctic charr (Salvelinus alpinus): The regulatory role of brain monoamines and pro-opiomelanocortin-derived peptides. J Exp Biol 203:1711–1721. https://doi.org/10.1242/jeb.203.11.1711
doi: 10.1242/jeb.203.11.1711
pubmed: 10804161
Jovanovic H, Perski A, Berglund H, Savic I (2011) Chronic stress is linked to 5-HT
doi: 10.1016/j.neuroimage.2010.12.060
pubmed: 21211567
Joy KP, Khan IA (1991) Pineal-gonadal relationship in the teleost Channa punctatus (Bloch): Evidence for possible involvement of hypothalamic serotonergic system. J Pineal Res 11:12–22. https://doi.org/10.1111/j.1600-079x.1991.tb00821.x
doi: 10.1111/j.1600-079x.1991.tb00821.x
pubmed: 1834824
Koski SE (2014) Broader horizons for animal personality research. Front Ecol Evol 2:70. https://doi.org/10.3389/fevo.2014.00070
doi: 10.3389/fevo.2014.00070
Lalley PM (1986) Serotoninergic and non-serotoninergic responses of phrenic motoneurones to raphe stimulation in the cat. J Physiol 380:373–385. https://doi.org/10.1113/jphysiol.1986.sp016291
doi: 10.1113/jphysiol.1986.sp016291
pubmed: 3612566
pmcid: 1182943
Lefrancois C, Shingles A, Domenici P (2005) The effect of hypoxia on locomotor performance and behaviour during escape in Liza aurata. J Fish Biol 67:1711–1729. https://doi.org/10.1111/j.1095-8649.2005.00884.x
doi: 10.1111/j.1095-8649.2005.00884.x
Lepage O, Larson ET, Mayer I, Winberg S (2005) Serotonin, but not melatonin, plays a role in shaping dominant-subordinate relationships and aggression in rainbow trout. Horm Behav 48:233–242. https://doi.org/10.1016/j.yhbeh.2005.02.012
doi: 10.1016/j.yhbeh.2005.02.012
pubmed: 15896794
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am Nat 153:649–659. https://doi.org/10.1086/303202
doi: 10.1086/303202
pubmed: 29585647
Liu C, Zhang W, Jiang P, Yv L, Lu W (2022) The anti-stress effect of taurine in fish: assessments based on repeat acute stress and animal individuality. Aquaculture 561:738685. https://doi.org/10.1016/j.aquaculture.2022.738685
Liu J, Wei X, Zhao C, Hu S, Duan J et al (2011) 5-HT induces enhanced phrenic nerve activity via 5-HT
doi: 10.1016/j.ejphar.2011.01.048
pubmed: 21296069
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Lopez-Patino MA, Skrzynska AK, Naderi F, Mancera JM, Miguez JM et al (2021) High stocking density and food deprivation increase brain monoaminergic activity in gilthead sea bream (Sparus aurata). Animals (Basel) 11. https://doi.org/10.3390/ani11061503
Martins CIM, Castanheira MF, Engrola S, Costas B, Conceição LEC (2011) Individual differences in metabolism predict coping styles in fish. Appl Anim Behav Sci 130:135–143. https://doi.org/10.1016/j.applanim.2010.12.007
doi: 10.1016/j.applanim.2010.12.007
Mathot KJ, Wright J, Kempenaers B, Dingemanse NJ (2012) Adaptive strategies for managing uncertainty may explain personality-related differences in behavioural plasticity. Oikos 121:1009–1020. https://doi.org/10.1111/j.1600-0706.2012.20339.x
doi: 10.1111/j.1600-0706.2012.20339.x
Maximino C, Lima MG, Costa CC, Guedes IML, Herculano AM (2014) Fluoxetine and WAY 100,635 dissociate increases in scototaxis and analgesia induced by conspecific alarm substance in zebrafish (Danio rerio Hamilton 1822). Pharmacol Biochem Behav 124:425–433. https://doi.org/10.1016/j.pbb.2014.07.003
doi: 10.1016/j.pbb.2014.07.003
pubmed: 25019652
McCrohan CR, Lu W, Brierley MJ, Dow L, Balment RJ (2007) Fish caudal neurosecretory system: A model for the study of neuroendocrine secretion. Gen Comp Endocrinol 153:243–250. https://doi.org/10.1016/j.ygcen.2006.12.027
doi: 10.1016/j.ygcen.2006.12.027
pubmed: 17316635
Medeiros LR, Mager EM, Grosell M, McDonald MD (2010) The serotonin subtype 1A receptor regulates cortisol secretion in the Gulf toadfish, Opsanus beta. Gen Comp Endocrinol 168:377–387. https://doi.org/10.1016/j.ygcen.2010.05.004
doi: 10.1016/j.ygcen.2010.05.004
pubmed: 20488186
Moberg GP, Mench JA (2000) The biology of animal stress: basic principles and implications for animal welfare. CABI, USA
doi: 10.1079/9780851993591.0000
Nelson RJ, Chiavegatto S (2002) Molecular basis of aggression. Trends Neurosci 24:713–719. https://doi.org/10.1016/s0166-2236(00)01996-2
doi: 10.1016/s0166-2236(00)01996-2
Olla BL, Davis MW, Schreck CB (1995) Stress-induced impairment of predator evasion and non-predator mortality in Pacific salmon. Aquac Res 26:393–398. https://doi.org/10.1111/j.1365-2109.1995.tb00928.x
doi: 10.1111/j.1365-2109.1995.tb00928.x
Olson EB, Dempsey JA, Mccrimmon D (1979) Serotonin and the control of ventilation in awake rats. J Clin Invest 64:689–693. https://doi.org/10.1172/JCI109510
doi: 10.1172/JCI109510
pubmed: 156738
pmcid: 372167
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. https://doi.org/10.1159/000006627
doi: 10.1159/000006627
pubmed: 10640786
Øverli Ø, Sørensen C, Nilsson GE (2006) Behavioral indicators of stress-coping style in rainbow trout: Do males and females react differently to novelty? Physiol Behav 87:506–512. https://doi.org/10.1016/j.physbeh.2005.11.012
doi: 10.1016/j.physbeh.2005.11.012
pubmed: 16455115
Øverli Ø, Sørensen C, Pulman KGT, Pottinger TG, Korzan W et al (2007) Evolutionary background for stress-coping styles: Relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412. https://doi.org/10.1016/j.neubiorev.2006.10.006
doi: 10.1016/j.neubiorev.2006.10.006
pubmed: 17182101
Øverli Ø, Winberg S, Damsård B, Jobling M (1998) Food intake and spontaneous swimming activity in Arctic char (Salvelinus alpinus): Role of brain serotonergic activity and social interactions. Can J Zool 76:1366–1370. https://doi.org/10.1139/cjz-76-7-1366
doi: 10.1139/cjz-76-7-1366
Roche DG, Taylor MK, Binning SA, Johansen JL, Domenici P et al (2014) Unsteady flow affects swimming energetics in a labriform fish (Cymatogaster aggregata). J Exp Biol 217:414–422. https://doi.org/10.1242/jeb.085811
doi: 10.1242/jeb.085811
pubmed: 24115060
Ruiz-Gomez MdL, Kittilsen S, Höglund E, Huntingford FA, Sørensen C et al (2008) Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: When doves become hawks. Horm Behav 54:534–538. https://doi.org/10.1016/j.yhbeh.2008.05.005
doi: 10.1016/j.yhbeh.2008.05.005
pubmed: 18632100
Rupia EJ, Binning SA, Roche DG, Lu W (2016) Fight-flight or freeze-hide? Personality and metabolic phenotype mediate physiological defence responses in flatfish. J Anim Ecol 85:927–937. https://doi.org/10.1111/1365-2656.12524
doi: 10.1111/1365-2656.12524
pubmed: 27044558
Rupia EJ, Zhao YJ, Lu WQ (2023) Individualities mediate divergent stress responses and appetite regulation in CNS of olive flounder, Paralichthys olivaceus. Aquaculture 563. https://doi.org/10.1016/j.aquaculture.2022.738957
Shoji H, Mizoguchi K (2011) Aging-related changes in the effects of social isolation on social behavior in rats. Physiol Behav 102:58–62. https://doi.org/10.1016/j.physbeh.2010.10.001
doi: 10.1016/j.physbeh.2010.10.001
pubmed: 20937292
Silva PIM, Martins CIM, Engrola S, Marino G, Øverli Ø et al (2010) Individual differences in cortisol levels and behaviour of Senegalese sole (Solea senegalensis) juveniles: Evidence for coping styles. Appl Anim Behav Sci 124:75–81. https://doi.org/10.1016/j.applanim.2010.01.008
doi: 10.1016/j.applanim.2010.01.008
Summers CH, Korzan WJ, Lukkes JL, Watt MJ, Forster GL et al (2005) Does serotonin influence aggression? Comparing regional activitybefore and during social interaction. Physiol Biochem Zool 78:679–694. https://doi.org/10.1086/432139
doi: 10.1086/432139
pubmed: 16059845
Trenzado CE, Carrick TR, Pottinger TG (2003) Divergence of endocrine and metabolic responses to stress in two rainbow trout lines selected for differing cortisol responsiveness to stress. Gen Comp Endocrinol 133:332–340. https://doi.org/10.1016/s0016-6480(03)00191-6
doi: 10.1016/s0016-6480(03)00191-6
pubmed: 12957477
Winberg S, Lepage O (1998) Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. Am J Physiol 274:R645-654. https://doi.org/10.1152/ajpregu.1998.274.3.R645
doi: 10.1152/ajpregu.1998.274.3.R645
pubmed: 9530229
Winberg S, Nilsson A, Hylland P, Soderstom V, Nilsson GE (1997a) Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish. Neurosci Lett 230:113–116. https://doi.org/10.1016/s0304-3940(97)00488-6
doi: 10.1016/s0304-3940(97)00488-6
pubmed: 9259477
Winberg S, Nilsson A, Hylland P, Söderstöm V, Nilsson GE (1997b) Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish. Neurosci Lett 230:113–116. https://doi.org/10.1016/S0304-3940(97)00488-6
doi: 10.1016/S0304-3940(97)00488-6
pubmed: 9259477
Winberg S, Nilsson GE (1993) Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp Biochem Physiol C 106:597–614. https://doi.org/10.1016/0742-8413(93)90216-8
doi: 10.1016/0742-8413(93)90216-8
Zeng J, Herbert NA, Lu W (2019) Differential coping strategies in response to salinity challenge in olive flounder. Front Physiol 10:1378. https://doi.org/10.3389/fphys.2019.01378
doi: 10.3389/fphys.2019.01378
pubmed: 31780952
pmcid: 6852876
Zou H, He F, Lan Z, Tang L, Lu W (2019) The personality of Japanese flounder (Paralichthys olivaceus) and gene expression related with osmoregulatory capacity in the gills. Aquaculture 500:221–227. https://doi.org/10.1016/j.aquaculture.2018.10.013
Zou H, Shi M, Li R, Zhang X, Lu W (2021) Comparative transcriptome and methylome analysis of the hindbrain in olive flounder (Paralichthys olivaceus ) considering individual behavior-type and oxygen metabolism. Comp Biochem Physiol D 38:100799. https://doi.org/10.1016/j.cbd.2021.100799
doi: 10.1016/j.cbd.2021.100799