Advertisement

Journal of Comparative Physiology A

, Volume 205, Issue 6, pp 867–880 | Cite as

Dietary l-tryptophan modulates agonistic behavior and brain serotonin in male dyadic contests of a cichlid fish

  • L. Morandini
  • M. R. Ramallo
  • M. F. Scaia
  • C. Höcht
  • G. M. Somoza
  • M. PandolfiEmail author
Original Paper
  • 51 Downloads

Abstract

Although some studies have investigated the effects of dietary l-tryptophan on agonistic behavior, research on adult fish specimens is still lacking. Moreover, submissive behaviors have been generally overlooked. We focused on agonistic behavior between males of the cichlid fish Cichlasoma dimerus, in dyadic encounters held in a novel context after being fed or not with an l-tryptophan enriched diet (TRP) for 2 weeks. We arranged three different dyads: control/control (control conditions: not TRP enriched), control/TRP, and TRP/TRP. We also registered the response of the brain serotonergic system in four brain regions. TRP/TRP dyads showed higher latencies to first attack, lower overall aggression, and lower proportions of bites and passive copings (submissive display) compared to control/control. TRP dominant males performed fewer bites with respect to controls, and subordinate males opposed to TRP males showed fewer passive copings. Higher serotonergic activities were found in subordinates’ optic tectum and in the telencephalon and preoptic area/hypothalamus of TRP males. Altogether, results point out that dietary l-tryptophan reduced males’ motivation to attack and dominant aggression, which consequently influenced subordinate agonistic repertory. In addition, males within TRP/TRP dyads showed a switch in their behavioral agonistic repertory. These behavioral outcomes were probably due to modifications at brain serotonergic functioning.

Keywords

Agonistic behavior Brain Cichlids l-Tryptophan Serotonin 

Abbreviations

5-HIAA

5-Hydroxyindoleacetic

5-HT

Serotonin

Bs

Brainstem

CTL

Control dietary protocol

CT

CTL vs. TRP male

CC

CTL vs. CTL male

DOM

Dominant

Lt

Total body length

Ot

Optic tectum

Poa/Hyp

Preoptic area/hypothalamus

SUB

Subordinate

Tel

Telencephalon

Trp

l-Tryptophan

TRP

l-Tryptophan supplemented dietary protocol

TT

TRP vs. TRP male

Notes

Acknowledgements

Our research has been funded by the following grants: Agencia de Promoción Científica y Tecnológica (Grant PICT 1482) and Universidad de Buenos Aires (Grant UBACyT 20020130200038BA). We would particularly like to thank Mariel Tripoli for her statistical recommendations and two anonymous reviewers for numerous meaningful suggestions.

Complaince with ethical standards

Ethical standards

All experiments were conducted in conformity with international standards on animal welfare, as well as being in accordance to institutional (Comisión Institucional para el Cuidado y Uso de Animales de Laboratorio, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires) and national (Comité Nacional de Ética en la Ciencia y la Tecnología, MINCyT, Argentina) regulations. All procedures were in compliance with the Guide for Care and Use of Laboratory Animals (National Research Council 2011).

References

  1. Aguiar A, Giaquinto PC (2018) Low cholesterol is not always good: low cholesterol levels are associated with decreased serotonin and increased aggression in fish. Biol Open 7(12):bio030981PubMedPubMedCentralGoogle Scholar
  2. Alcazar RM, Hilliard AT, Becker L, Bernaba M, Fernald RD (2014) Brains over brawn: experience overcomes a size disadvantage in fish social hierarchies. J Exp Biol 217:1462–1468PubMedPubMedCentralGoogle Scholar
  3. Almirón AE, Casciotta JR, Ciotek L, Giorgis P (2015) Guía de los Peces del Parque Nacional Pre-Delta. Administración de Parques Nacionales, Ciudad Autónoma de Buenos AiresGoogle Scholar
  4. Alonso F, Honji RM, Moreira RG, Pandolfi M (2012) Dominance hierarchies and social status ascent opportunity: anticipatory behavioral and physiological adjustments in a Neotropical cichlid fish. Physiol Behav 106:612–618PubMedGoogle Scholar
  5. Angus D, Schutter DJ, Terburg D, van Honk J, Harmon-Jones E (2016) A review of social neuroscience research on anger and aggression. In: Harmon-Jones E, Inzlicht M (eds) Social neuroscience: biological approaches to social psychology. Routledge, New York, pp 223–246Google Scholar
  6. Arnott G, Elwood RW (2008) Information gathering and decision making about resource value in animal contests. Anim Behav 76:529–542Google Scholar
  7. Audero E, Mlinar B, Baccini G, Skachokova ZK, Corradetti R, Gross C (2013) Suppression of serotonin neuron firing increases aggression in mice. J Neurosci 33:8678–8688PubMedPubMedCentralGoogle Scholar
  8. Baduy F, Guerreiro PM, Canário AV, Saraiva JL (2017) Social organization and endocrine profiles of Australoheros facetus, an exotic freshwater fish in southern Portugal. Acta Ethol 20:263–277Google Scholar
  9. Basic D, Krogdahl Å, Schjolden J, Winberg S, Vindas MA, Hillestad M, Mayer I, Skjerve E, Höglund E (2013) Short-and long-term effects of dietary l-tryptophan supplementation on the neuroendocrine stress response in seawater-reared Atlantic salmon (Salmo salar). Aquacul 388:8–13Google Scholar
  10. Beaugrand J, Goulet C, Payette D (1991) Outcome of dyadic conflict in male green swordtail fish, Xiphophorus helleri: effects of body size and prior dominance. Anim Behav 41:417–424Google Scholar
  11. Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507Google Scholar
  12. Bjork JM, Dougherty DM, Moeller FG, Cherek DR, Swann AC (1999) The effects of tryptophan depletion and loading on laboratory aggression in men: time course and a food-restricted control. Psychopharmacology 142:24–30PubMedGoogle Scholar
  13. Briffa M, Sneddon LU, Wilson AJ (2015) Animal personality as a cause and consequence of contest behaviour. Biol Lett 11:20141007PubMedPubMedCentralGoogle Scholar
  14. Castanheira MF, Herrera M, Costas B, Conceição LE, Martins CI (2013) Linking cortisol responsiveness and aggressive behaviour in gilthead seabream Sparus aurata: indication of divergent coping styles. Appl Anim Behav Sci 143:75–81Google Scholar
  15. Chamberlain B, Ervin F, Pihl RO, Young SN (1987) The effect of raising or lowering tryptophan levels on aggression in vervet monkeys. Pharmacol Biochem Behav 27:503–510Google Scholar
  16. Clinard CT, Barnes AK, Adler SG, Cooper MA (2016) Winning agonistic encounters increases testosterone and androgen receptor expression in Syrian hamsters. Horm Behav 86:27–35PubMedPubMedCentralGoogle Scholar
  17. Crothers LR, Cummings ME (2015) A multifunctional warning signal behaves as an agonistic status signal in a poison frog. Behav Ecol 26:560–568Google Scholar
  18. Cubitt KF, Winberg S, Huntingford FA, Kadri S, Crampton VO, Øverli Ø (2008) Social hierarchies, growth and brain serotonin metabolism in Atlantic salmon (Salmo salar) kept under commercial rearing conditions. Physiol Behav 94:529–535PubMedGoogle Scholar
  19. Dahlbom SJ, Backström T, Lundstedt-Enkel K, Winberg S (2012) Aggression and monoamines: effects of sex and social rank in zebrafish (Danio rerio). Behav Brain Res 228:333–338PubMedGoogle Scholar
  20. DeNapoli JS, Dodman NH, Shuster L, Rand WM, Gross KL (2000) Effect of dietary protein content and tryptophan supplementation on dominance aggression, territorial aggression, and hyperactivity in dogs. J Am Vet Med Assoc 217:504–508PubMedGoogle Scholar
  21. Dijkstra PD, Schaafsma SM, Hofmann HA, Groothuis TG (2012) ‘Winner effect’ without winning: unresolved social conflicts increase the probability of winning a subsequent contest in a cichlid fish. Physiol Behav 105:489–492PubMedGoogle Scholar
  22. Dorelle LS, Da Cuña RH, Vázquez GR, Höcht C, Shimizu A, Genovese G, Nostro FLL (2017) The SSRI fluoxetine exhibits mild effects on the reproductive axis in the cichlid fish Cichlasoma dimerus (Teleostei, Cichliformes). Chemosphere 171:370–378PubMedGoogle Scholar
  23. Duke AA, Bègue L, Bell R, Eisenlohr-Moul T (2013) Revisiting the serotonin–aggression relation in humans: a meta-analysis. Psychol Bull 139:1148PubMedPubMedCentralGoogle Scholar
  24. Favati A, Leimar O, Radesäter T, Løvlie H (2014) Social status and personality: stability in social state can promote consistency of behavioural responses. Proc R Soc Lond B Biol Sci 281:20132531Google Scholar
  25. Fernstrom JD, Wurtman RJ (1971) Brain serotonin content: physiological dependence on plasma tryptophan levels. Science 173:149–152PubMedGoogle Scholar
  26. Filby AL, Paull GC, Hickmore TF, Tyler CR (2010) Unravelling the neurophysiological basis of aggression in a fish model. BMC Genomics 11(781):498PubMedPubMedCentralGoogle Scholar
  27. Frost AJ, Winrow-Giffen A, Ashley PJ, Sneddon LU (2007) Plasticity in animal personality traits: does prior experience alter the degree of boldness? Proc R Soc Lond B Biol Sci 274:333–339Google Scholar
  28. Fulton TW (1904) The rate of growth of fishes. Twenty-second Annual Report, Part III. Fisheries Board of Scotland, Edinburgh, pp 141–241Google Scholar
  29. Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48:11–22PubMedPubMedCentralGoogle Scholar
  30. Haller J (2014) The glucocorticoid/aggression relationship in animals and humans: an analysis sensitive to behavioral characteristics, glucocorticoid secretion patterns, and neural mechanisms. In: Miczek KA, Meyer-Lindenberg A (eds) Neuroscience of aggression. Springer, Heidelberg, pp 73–109Google Scholar
  31. Haller J, Harold G, Sandi C, Neumann ID (2014) Effects of adverse early life events on aggression and anti-social behaviours in animals and humans. J Endocrinol 26:724–738Google Scholar
  32. Herrero L, Rodriguez F, Salas C, Torres B (1998) Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120:291–305PubMedGoogle Scholar
  33. Higuchi Y, Soga T, Parhar IS (2018) Social defeat stress decreases mRNA for monoamine oxidase A and increases 5-HT turnover in the brain of male nile tilapia (Oreochromis niloticus). Front Pharmacol 9:1549PubMedGoogle Scholar
  34. 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 249:525–531Google Scholar
  35. Hoseini SM, Pérez-Jiménez A, Costas B, Azeredo R, Gesto M (2019) Physiological roles of tryptophan in teleosts: current knowledge and perspectives for future studies. Rev Aquacult 11:3–24Google Scholar
  36. Johnston WL, Atkinson JL, Hilton JW, Were KE (1990) Effect of dietary tryptophan on plasma and brain tryptophan, brain serotonin, and brain 5-hydroxyindoleacetic acid in rainbow trout. J Nutr Biochem 1:49–54PubMedGoogle Scholar
  37. Kaslin J, Panula P (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J Comp Neurol 440:342–377PubMedGoogle Scholar
  38. Kokko H (2013) Dyadic contests: modelling fights between two individuals. In: Hardy IC, Briffam M (eds) Animal contests. Cambridge University Press, Cambridge, pp 5–32Google Scholar
  39. Koolhaas JM, De Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307–321PubMedGoogle Scholar
  40. Lan YT, Hsu Y (2011) Prior contest experience exerts a long-term influence on subsequent winner and loser effects. Front Zool 8:28PubMedPubMedCentralGoogle Scholar
  41. Larson ET, Summers CH (2001) Serotonin reverses dominant social status. Behav Brain Res 121:95–102PubMedGoogle Scholar
  42. Larson ET, O’Malley DM, Melloni RH (2006) Aggression and vasotocin are associated with dominant–subordinate relationships in zebrafish. Behav Brain Res 167:94–102PubMedGoogle Scholar
  43. Lehtonen TK, Svensson PA, Wong BB (2016) The influence of recent social experience and physical environment on courtship and male aggression. BMC Evol Biol 16:18PubMedPubMedCentralGoogle Scholar
  44. Lenkov K, Lee MH, Lenkov OD, Swafford A, Fernald RD (2015) Epigenetic DNA methylation linked to social dominance. PLoS ONE 10:e0144750PubMedPubMedCentralGoogle Scholar
  45. Lepage O, Tottmar O, Winberg S (2002) Elevated dietary intake of tryptophan counteracts the stress-induced elevation of plasma cortisol in rainbow trout (Oncorhynchus mykiss). J Exp Biol 205:3679–3687PubMedGoogle Scholar
  46. Lepage O, Vílchez IM, Pottinger TG, Winberg S (2003) Time course of the effect of dietary l-tryptophan on plasma cortisol levels in rainbow trout Oncorhynchus mykiss. J Exp Biol 206:3589–3599PubMedGoogle Scholar
  47. 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 48:233–242PubMedGoogle Scholar
  48. Li YZ, Kerr BJ, Kidd MT, Gonyou HW (2006) Use of supplementary tryptophan to modify the behavior of pigs. J Anim Sci 84:212–220PubMedGoogle Scholar
  49. Ligon RA (2014) Defeated chameleons darken dynamically during dyadic disputes to decrease danger from dominants. Behav Ecol Sociobiol 68:1007–1017Google Scholar
  50. Loveland JL, Uy N, Maruska KP, Carpenter RE, Fernald RD (2014) Social status differences regulate the serotonergic system of a cichlid fish, Astatotilapia burtoni. J Exp Biol 217:2680–2690PubMedPubMedCentralGoogle Scholar
  51. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedPubMedCentralGoogle Scholar
  52. Maruska KP, Becker L, Neboori A, Fernald RD (2013) Social descent with territory loss causes rapid behavioral, endocrine and transcriptional changes in the brain. J Exp Biol 216:3656–3666PubMedPubMedCentralGoogle Scholar
  53. McDonald MD (2017) An AOP analysis of selective serotonin reuptake inhibitors (SSRIs) for fish. Comp Biochem Physiol C: Toxicol Pharmacol 197:19–31Google Scholar
  54. Mir JI, Shabir R, Mir FA (2012) Length-weight relationship and condition factor of Schizopyge curvifrons (Heckel, 1838) from River Jhelum, Kashmir, India. World J Fish Mar Sci 4:325–329Google Scholar
  55. Morandini L, Ramallo MR, Moreira RG, Höcht C, Somoza GM, Silva A, Pandolfi M (2015) Serotonergic outcome, stress and sexual steroid hormones, and growth in a South American cichlid fish fed with an l-tryptophan enriched diet. Gen Comp Endocrinol 223:27–37PubMedGoogle Scholar
  56. Muchlisin ZA, Musman M, Siti Azizah MN (2010) Length-weight relationships and condition factors of two threatened fishes, Rasbora tawarensis and Poropuntius tawarensis, endemic to Lake Laut Tawar, Aceh Province, Indonesia. J Appl Ichthyol 26:949–953Google Scholar
  57. National Research Council (2011) Guide for the care and use of laboratory animals. The National Academies Press, Washington, DCGoogle Scholar
  58. Neat FC, Huntingford FA, Beveridge MM (1998) Fighting and assessment in male cichlid fish: the effects of asymmetries in gonadal state and body size. Anim Behav 55:883–891PubMedGoogle Scholar
  59. Neff NH, Tozer TN (1968) In vivo measurement of brain serotonin turnover. Adv Pharmacol 6:97–109PubMedGoogle Scholar
  60. Nelson RJ, Trainor BC (2007) Neural mechanisms of aggression. Nat Rev Neurosci 8:536–546PubMedGoogle Scholar
  61. Oliveira RF, Simões JM, Teles MC, Oliveira CR, Becker JD, Lopes JS (2016) Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain. Proc Natl Acad Sci USA 113(5):E654–E661PubMedGoogle Scholar
  62. Øverli Ø, Pottinger TG, Carrick TR, Øverli E, Winberg S (2002) Differences in behaviour between rainbow trout selected for high-and low-stress responsiveness. J Exp Biol 205:391–395PubMedGoogle Scholar
  63. Øverli Ø, Korzan WJ, Höglund E, Winberg S, Bollig H, Watt M, Forster GL, Barton BA, Øverli E, Renner KJ, Summers CH (2004) Stress coping style predicts aggression and social dominance in rainbow trout. Horm Behav 45:235–241PubMedGoogle Scholar
  64. Pan Y, Xu L, Young KA, Wang Z, Zhang Z (2010) Agonistic encounters and brain activation in dominant and subordinate male greater long-tailed hamsters. Horm Behav 58:478–484PubMedPubMedCentralGoogle Scholar
  65. Pellis SM, Pellis VC (2015) Are agonistic behavior patterns signals or combat tactics—or does it matter? Targets as organizing principles of fighting. Physiol Behav 146:73–78Google Scholar
  66. Ramallo MR, Morandini L, Alonso F, Birba A, Tubert C, Fiszbein A, Pandolfi M (2014) The endocrine regulation of cichlids social and reproductive behavior through the eyes of the chanchita, Cichlasoma dimerus (Percomorpha; Cichlidae). J Physiol Paris 108:194–202PubMedGoogle Scholar
  67. Ramallo MR, Birba A, Honji RM, Morandini L, Moreira RG, Somoza GM, Pandolfi M (2015) A multidisciplinary study on social status and the relationship between inter-individual variation in hormone levels and agonistic behavior in a Neotropical cichlid fish. Horm Behav 69:139–151PubMedGoogle Scholar
  68. Scaia MF, Morandini L, Noguera CA, Ramallo MR, Somoza GM, Pandolfi M (2018) Fighting cichlids: dynamic of intrasexual aggression in dyadic agonistic encounters. Behav Process 147:61–69Google Scholar
  69. Serra M, Wolkers CPB, Urbinati EC (2015) Novelty of the arena impairs the cortisol-related increase in the aggression of matrinxã (Brycon amazonicus). Physiol Behav 141:51–57PubMedGoogle Scholar
  70. Shannon NJ, Gunnet JW, Moore KE (1986) A comparison of biochemical indices of 5-hydroxytryptaminergic neuronal activity following electrical stimulation of the dorsal raphe nucleus. J Neurochem 47:958–965PubMedGoogle Scholar
  71. Shea MM, Douglass LW, Mench JA (1991) The interaction of dominance status and supplemental tryptophan on aggression in Gallus domesticus males. Phamaracol Biochem Behav 38:587–591Google Scholar
  72. Stamps JA (2016) Individual differences in behavioural plasticities. Biol Rev 91:534–567PubMedGoogle Scholar
  73. Summers CH, Korzan WJ, Lukkes JL, Watt MJ, Forster GL, Øverli Ø, Höglund E, Larson ET, Ronan PJ, Matter JM, Summers TR, Renner KJ, Greenberg N (2005) Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiol Biochem Zool 78:679–694PubMedGoogle Scholar
  74. Teles MC, Dahlbom SJ, Winberg S, Oliveira RF (2013) Social modulation of brain monoamine levels in zebrafish. Behav Brain Res 253:17–24PubMedGoogle Scholar
  75. Teles MC, Cardoso SD, Oliveira RF (2016) Social plasticity relies on different neuroplasticity mechanisms across the brain social decision-making network in zebrafish. Front Behav Neurosci 10:16PubMedPubMedCentralGoogle Scholar
  76. Tubert C, Lo Nostro FL, Villafañe MV, Pandolfi M (2012) Aggressive behavior and reproductive physiology in females of the social cichlid fish Cichlasoma dimerus. Physiol Behav 106:193–200PubMedGoogle Scholar
  77. van Raaij MT, Pit DS, Balm PH, Steffens AB, van den Thillart GE (1996) Behavioral strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Horm Behav 30:85–92PubMedGoogle Scholar
  78. Veenema AH (2009) Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front Neuroendocrinol 30:497–518PubMedGoogle Scholar
  79. Wazlavek BE, Figler MH (1989) Territorial prior residence, size asymmetry, and escalation of aggression in convict cichlids (Cichlasoma nigrofasciatum Günther). Aggress Behav 15:235–244Google Scholar
  80. Winberg S, Nilsson GE (1993) Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp Biochem Physiol A: Mol Integr Physiol 106:597–614Google Scholar
  81. Winberg S, Thörnqvist PO (2016) Role of brain serotonin in modulating fish behavior. Curr Zool 62:317–323PubMedPubMedCentralGoogle Scholar
  82. Winberg S, Nilsson GE, Olsén KH (1991) Social rank and brain levels of monoamines and monoamine metabolites in Arctic charr, Salvelinus alpinus (L.). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 168:241–246Google Scholar
  83. Winberg S, Øverli Ø, Lepage O (2001) Suppression of aggression in rainbow trout (Oncorhynchus mykiss) by dietary l-tryptophan. J Exp Biol 204:3867–3876PubMedGoogle Scholar
  84. Wolkers CPB, Serra M, Hoshiba MA, Urbinati EC (2012) Dietary l-tryptophan alters aggression in juvenile matrinxã Brycon amazonicus. Fish Physiol Biochem 38:819–827PubMedGoogle Scholar
  85. Wolkers CPB, Serra M, Szawka RE, Urbinati EC (2014) The time course of aggressive behaviour in juvenile matrinxã Brycon amazonicus fed with dietary l-tryptophan supplementation. J Fish Biol 84:45–57PubMedGoogle Scholar
  86. Wolkers CPB, Serra M, Urbinati EC (2015) Social challenge increases cortisol and hypothalamic monoamine levels in matrinxã (Brycon amazonicus). Fish Phyisiol Biochem 41:1501–1508Google Scholar
  87. Yanowitch R, Coccaro EF (2011) The neurochemistry of human aggression. Adv Genet 75:151–169PubMedGoogle Scholar
  88. Young SN (2013) The effect of raising and lowering tryptophan levels on human mood and social behavior. Philos Trans Soc Lond B Biol Sci 368:20110375Google Scholar
  89. Young SN, Gauthier S (1981) Effect of tryptophan administration on tryptophan, 5-hydroxyindoleacetic acid and indoleacetic acid in human lumbar and cisternal cerebrospinal fluid. J Neurol Neurosurg Psychiatry 44:323–328PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • L. Morandini
    • 1
  • M. R. Ramallo
    • 1
  • M. F. Scaia
    • 1
  • C. Höcht
    • 2
  • G. M. Somoza
    • 3
  • M. Pandolfi
    • 1
    Email author
  1. 1.Laboratorio de Neuroendocrinología y ComportamientoDBBE, FCEN, UBA e IBBEA, CONICET-UBABuenos AiresArgentina
  2. 2.Departamento de Farmacología, Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresBuenos AiresArgentina
  3. 3.Instituto Tecnológico de Chascomús (CONICET-UNSAM)Buenos AiresArgentina

Personalised recommendations