Abstract
Fish that display schooling and social behaviors are expected to show stress responses when they are challenged by isolation. Medaka exhibit social behavior in group situations, but little is known about the effects of social isolation on their physiological stress responses. Here, we subjected male medaka to several different housing situations and assessed whether the stress responses differed between grouped and isolated fish. Social isolation decreased plasma cortisol and increased brain serotonin [5-hydroxytryptamine (5-HT)] levels in male medaka irrespective of whether or not the isolated fish could visually perceive another individual. However, heat shock treatment, a grouped situation, and a paired situation increased plasma cortisol and decreased brain 5-HT levels. These results suggest that, in male medaka, physical contact among individuals is more stressful than isolation. Moreover, both grouped and paired fish had lower tryptophan hydroxylase 2 (Tph2) expression levels than isolated fish, whereas heat shock downregulated both Tph1 and Tph2. The present study indicates that, in fish, the magnitude of reduction in brain Tph1 and Tph2 expression levels and serotonin concentration varies with the type of stress.
Similar content being viewed by others
References
Almeida O, Gonçalves-de-Freitas E, Lopes JS, Oliveira RF (2014) Social instability promotes hormone–behavior associated patterns in a cichlid fish. Horm Behav 66:369–382
Ansai S, Hosokawa H, Maegawa S, Kinoshita M (2016) Chronic fluoxetine treatment induces anxiolytic responses and altered social behaviors in medaka, Oryzias latipes. Behav Brain Res 303:126–136
Ansai S, Hosokawa H, Maegawa S, Naruse K, Washio Y, Sato K, Kinoshita M (2017) Deficiency of serotonin in raphe neurons and altered behavioral responses in tryptophan hydroxylase 2-knockout medaka (Oryzias latipes). Zebrafish 14:495–507
Arends RJ, Mancera JM, Munõz JL, Wendelaar Bonga SE, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocrinol 163:149–157
Basu N, Nakano T, Grau EG, Iwama GK (2001) The effects of cortisol on heat shock protein 70 levels in two fish species. Gen Comp Endocrinol 124:97–105
Brain PF, Nowell NW (1971) Isolation versus grouping effects on adrenal and gonadal function in albino mice. I. The male. Gen Comp Endocrinol 16:149–154
Burmeister SS, Wilczynski W (2005) Social signals regulate gonadotropin-releasing hormone neurons in the green treefrog. Brain Behav Evol 65:26–32
Clotfelter ED, Paolino AD (2003) Bystanders to contests between conspecifics are primed for increased aggression in male fighting fish. Anim Behav 66:343–347
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 228:333–338
Dong XZ, Li ZL, Zheng XL, Mu LH, Zhang G, Liu P (2013) A representative prescription for emotional disease, Ding-Zhi-Xiao-Wan restores 5-HT system deficit through interfering the synthesis and transshipment in chronic mild stress-induced depressive rats. J Ethnopharmacol 150:1053–1061
Earley RL, Edwards JT, Aseem O, Felton K, Blumer LS, Karom M, Grober MS (2006) Social interactions tune aggression and stress responsiveness in a territorial cichlid fish (Archocentrus nigrofasciatus). Physiol Behav 88:353–363
Forsatkar MN, Safari O, Boiti C (2017) Effects of social isolation on growth, stress response, and immunity of zebrafish. Acta Ethol 20:255–261
Fukamachi S, Kinoshita M, Aizawa K, Oda S, Meyer A, Mitani H (2009) Dual control by a single gene of secondary sexual characters and mating preferences in medaka. BMC Biol. https://doi.org/10.1186/1741-7007-7-64
Galhardo L, Oliveira RF (2014) The effects of social isolation on steroid hormone levels are modulated by previous social status and context in a cichlid fish. Horm Behav 65:1–5
Giacomini ACVV, de Abreu MS, Koakoski G, Idalêncio R, Kalichak F, Oliveira TA, da Rosa JGS, Gusso D, Piato AL, Barcellos LJG (2015) My stress, our stress: blunted cortisol response to stress in isolated housed zebrafish. Physiol Behav 139:182–187
Gómez-Laplaza LM, Morgan E (1991) Effects of short-term isolation on the locomotor activity of the angelfish (Pterophyllum scalare). J Comp Psychol 105:366–375
Guesdon V, Meurisse M, Chesneau D, Picard S, Lévy F, Chaillou E (2015) Behavioral and endocrine evaluation of the stressfulness of single-pen housing compared to group-housing and social isolation conditions. Physiol Behav 147:63–70
Hannes RP, Franck D (1983) The effect of social isolation on androgen and corticosteroid levels in a cichlid fish (Haplochromis burtoni) and in swordtails (Xiphophorus helleri). Horm Behav 17:292–301
Heynen M, Backström T, Fick J, Jonsson M, Klaminder J, Brodin T (2016) Home alone—the effects of isolation on uptake of a pharmaceutical contaminant in a social fish. Aquat Toxicol 180:71–77
Imada H, Hoki M, Suehiro Y, Okuyama T, Kurabayashi D, Shimada A et al (2010) Coordinated and cohesive movement of two small conspecific fish induced by eliciting a simultaneous optomotor response. PLOS ONE 5:e11248
Kagawa N (2013) Social rank-dependent expression of arginine vasotocin in distinct preoptic regions in male Oryzias latipes. J Fish Biol 82:354–363
Kagawa N (2014) Comparison of aggressive behaviors between two wild populations of Japanese medaka, Oryzias latipes and O. sakaizumii. Zool Sci 31:116–121
Kagawa N, Mugiya Y (2000) Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels. Zool Sci 17:1061–1066
Kagawa N, Hirose S, Fujimoto K, Nomura C, Fujita Y, Honda A, Komori M (2017) Social rank-dependent expression of gonadotropin-releasing hormones and kisspeptin in the medaka brain. Gen Comp Endocrinol 249:48–54
Kanitz E, Tuchscherer M, Puppe B, Tuchscherer A, Stabenow B (2004) Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain Behav Immun 18:35–45
Khan IA, Thomas P (1993) Immunocytochemical localization of serotonin and gonadotropin-releasing hormone in the brain and pituitary gland of the Atlantic croaker Micropogonias undulates. Gen Comp Endocrinol 91:167–180
Laursen DC, Silva PIM, Larsen BK, Höglund E (2013) High oxygen consumption rates and scale loss indicate elevated aggressive behaviour at low rearing density, while elevated brain serotonergic activity suggests chronic stress at high rearing densities in farmed rainbow trout. Physiol Behav 122:147–154
Mosienko V, Bert B, Beis D, Matthes S, Fink H, Bader M et al (2012) Exaggerated aggression and decreased anxiety in mice deficient in brain serotonin. Transl Psychiatry. https://doi.org/10.1038/tp.2012.44
Nakayama K, Oshima Y, Hiramatsu K, Shimasaki Y, Honjo T (2005) Effects of polychlorinated biphenyls on the schooling behavior of Japanese medaka (Oryzias latipes) Environ. Toxicol Chem 24:2588–2593
Ochiai T, Suehiro Y, Nishinari K, Kubo T, Takeuchi H (2013) A new data-mining method to search for behavioral properties that induce alignment and their involvement in social learning in medaka fish (Oryzias latipes). PLOS ONE 8:e71685
Otsuka A, Shimomura K, Niwa H, Kagawa N (2020) The presence of a conspecific induces risk-taking behaviour and enlargement of somata size of dopaminergic neurons in the brain of male medaka fish. J Fish Biol. https://doi.org/10.1111/jfb.14293
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
Parker MO, Millington ME, Combe FJ, Brennan CH (2012) Housing conditions differentially affect physiological and behavioural stress responses of zebrafish, as well as the response to anxiolytics. PLOS ONE 7:e34992
Perveen T, Emad S, Haider S, Sadaf S, Qadeer S, Batool Z et al (2018) Role of cyclooxygenase inhibitors in diminution of dissimilar stress-induced depressive behavior and memory impairment in rats. Neurosci 370:121–129
Pickering AD (1992) Rainbow trout husbandry: management of the stress response. Aquaculture 100:125–139
Pottinger TG (1998) Changes in blood cortisol, glucose and lactate in carp retained in anglers’ keepnets. J Fish Biol 53:728–742
Rahman MS, Thomas P (2009) Molecular cloning, characterization and expression of two tryptophan hydroxylase (TPH-1 and TPH-2) genes in the hypothalamus of Atlantic croaker: down-regulation after chronic exposure to hypoxia. Neuroscience 158:751–765
Rahman MS, Thomas P (2014) Restoration of tryptophan hydroxylase functions and serotonin content in the Atlantic croaker hypothalamus by antioxidant treatment during hypoxic stress. Front Neurosci. https://doi.org/10.3389/fnins.2014.00130
Reuss S (1996) Components and connections of the circadian timing system in mammals. Cell Tissue Res 285:353–378
Senthilkumaran B, Okuzawa K, Gen K, Kagawa H (2001) Effects of serotonin, GABA and neuropeptide Y on seabream gonadotropin-releasing hormone release in vitro from preoptic—anterior hypothalamus and pituitary of red seabream, Pagrus major. J Neuroendocrinol 13:395–400
Serra M, Sanna E, Mostallino MC, Biggio G (2007) Social isolation stress and neuroactive steroids. Eur Neuropsychopharmacol 17:1–11
Shams S, Seguin D, Facciol A, Chatterjee D, Gerlai R (2017) Effect of social isolation on anxiety-related behaviors, cortisol, and monoamines in adult zebrafish. Behav Neurosci 131:492–504
Shimomura Y, Inahata M, Komori M, Kagawa N (2019) Reduction of tryptophan hydroxylase expression in the brain of medaka fish after repeated heat stress. Zool Sci 36:223–230
Silva PIM, Martins CIM, Khan UW, Gjøen HM, Øverli Ø, Höglund E (2015) Stress and fear responses in the teleost pallium. Physiol Behav 141:17–22
Sørensen C, Nilsson GE, Summers CH, Øverli Ø (2012) Social stress reduces forebrain cell proliferation in rainbow trout (Oncorhynchus mykiss). Behav Brain Res 227:311–331
Vijayan MM, Moon TW (1994) The stress response and the plasma disappearance of corticosteroid and glucose in a marine teleost, the sea raven. Can J Zool 72:379–386
Waring CP, Brown JA, Collins JE, Prunet P (1996) Plasma prolactin, cortisol, and thyroid responses of the brown trout (Salmo trutta) exposed to lethal and sublethal aluminium in acidic soft water. Gen Comp Endocrinol 102:377–385
Wolkers CPB, Serra M, Urbinati EC (2015) Social challenge increases cortisol and hypothalamic monoamine levels in matrinxã (Brycon amazonicus). Fish Physiol Biochem 41:1501–1508
Acknowledgment
This work was supported by the Japan Society for the Promotion of Science (grant no. 18K05833).
Author information
Authors and Affiliations
Contributions
A. O. and N. K. designed the study. A. O., M. I., and Y. S. performed the experiments and analyzed the data. A. O. and N. K. wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors have no competing interests to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Otsuka, A., Inahata, M., Shimomura, Y. et al. Physiological changes in response to social isolation in male medaka fish. Fish Sci 86, 775–781 (2020). https://doi.org/10.1007/s12562-020-01441-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-020-01441-1