Abstract
In fish, aggression has significant individual differences, and different personalities exhibit distinct behavioral performances and physiological stress responses. Under intensive culture conditions, Sebastes schlegelii juveniles display severe aggression and cannibalism, causing damage to fish welfare and economic loss. Herein, we investigated the alterations in behavioral performance and physiological stress indicators of Sebastes schlegelii juveniles with different aggressiveness. The results revealed that latency to the first movement, distance to center point, mobile frequency, and immobile frequency were significantly lower in high-aggressive individuals than low-aggressive individuals. In contrast, the immobile time was significantly higher in high-aggressive individuals compared to low-aggressive individuals. PCA was performed to identify the key parameters of fish behavior. From the results of PCA, position, motion state, and physical status could be used as behavioral screening indicators for individuals with different aggressiveness. The 5-HIAA/5-HT ratio was significantly lower in high-aggressive individuals than in low-aggressive individuals. Moreover, cortisol levels were positively correlated with immobile time, and the ratio of 5-HIAA/5-HT was significantly and positively correlated with the distance to the central point. These results suggested that individuals with different aggressiveness can be effectively distinguished in a short period of time according to behavioral factors such as position, motion state, and physical status. For a single measure, the distance to center point associated with brain monoaminergic activity may be a more direct factor. The results could be a non-invasive method to measure fish aggression and fish welfare, and then build on to improve fish welfare and enhance aquaculture management.
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References
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):bio030981. https://doi.org/10.1242/bio.030981
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(5):612–618. https://doi.org/10.1016/j.physbeh.2012.04.003.10.1016/j.physbeh.2012.04.003
Ariyomo TO, Carter M, Watt PJ (2013) Heritability of boldness and aggressiveness in the zebrafish. Behav Genet 43(2):161–167. https://doi.org/10.1007/s10519-013-9585-y
Backström T, Winberg S (2017) Serotonin coordinates responses to social stress-what we can learn from fish. Front Neurosci 11:595. https://doi.org/10.3389/fnins.2017.00595
Bessa E, Sadoul B, Mckenzie DJ, Geffroy B (2021) Group size, temperature and body size modulate the effects of social hierarchy on basal cortisol levels in fishes. Horm Behavior 136:105077. https://doi.org/10.1016/j.yhbeh.2021.105077
Boscolo CNP, Pereira TSB, Batalhão IG, Dourado PLR, Schlenk D, de Almeida EA (2018) Diuron metabolites act as endocrine disruptors and alter aggressive behavior in Nile tilapia (Oreochromis niloticus). Chemosphere 191:832–838. https://doi.org/10.1016/j.chemosphere.2017.10.009
Brandão ML, Colognesi G, Bolognesi MC, Costa-Ferreira RS, Carvalho TB, Gonçalves-de-Freitas E (2018) Water temperature affects aggressive interactions in a Neotropical cichlid fish. Neotrop Ichthyol 16(1). https://doi.org/10.1590/1982-0224-20170081.
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(1):75–81. https://doi.org/10.1016/j.applanim.2012.11.008
Cervantes MC, Delville Y (2007) Individual differences in offensive aggression in golden hamsters: a model of reactive and impulsive aggression? Neuroscience 150(3):511–521. https://doi.org/10.1016/j.neuroscience.2007.09.034
Clotfelter ED, O’Hare EP, McNitt MM, Carpenter RE, Summers CH (2007) Serotonin decreases aggression via 5-HT1A receptors in the fighting fish Betta splendens. Pharmacol Biochem Be 87(2):222–231. https://doi.org/10.1016/j.pbb.2007.04.018
Colléter M, Brown C (2011) Personality traits predict hierarchy rank in male rainbowfish social groups. Anim Behav 81(6):1231–1237. https://doi.org/10.1016/j.anbehav.2011.03.011
Dahlbom SJ, Lagman D, Lundstedt-Enkel K, Sundström LF, Winberg S (2011) Boldness predicts social status in zebrafish (Danio rerio). PLoS One 6(8):e23565. https://doi.org/10.1371/journal.pone.0023565
Dorfman HM, Meyer-Lindenberg A, Buckholtz JW (2013) Neurobiological mechanisms for impulsive-aggression: the role of MAOA. Neurosci Aggress 17:297–313. https://doi.org/10.1007/7854_2013_272
Ellis T, Yildiz HY, López-Olmeda J, Spedicato MT, Tort L, Øverli Ø, Martins CI (2012) Cortisol and finfish welfare. Fish Physiol Biochem 38(1):163–188. https://doi.org/10.1007/s10695-011-9568-y
Falsarella DNL, Brandão ML, Gonçalves-de-Freitas E (2017) Fish adjust aggressive behavior to audience size with limited information on bystanders’ fighting ability. Behav Process 142:116–118. https://doi.org/10.1016/j.beproc.2017.07.002
Fanning JR, Lee R, Coccaro EF (2020) Neurotransmitter function in impulsive aggression and intermittent explosive disorder. Wiley Int Handb Psychopathic Disord Law 249-269.https://doi.org/10.1002/9781119159322.ch10
Faught E, Vijayan MM (2016) Mechanisms of cortisol action in fish hepatocytes. Comp Biochem Phys B 199:136–145. https://doi.org/10.1016/j.cbpb.2016.06.012
Fontana BD, Meinerz DL, Rosa LVC, Mezzomo NJ, Silveira A, Giuliani GS, Quadros VA, Filho GLB, Blaser RE, Rosemberg DB (2016) Modulatory action of taurine on ethanol-induced aggressive behavior in zebrafish. Pharmacol Biochem Be 141:18–27. https://doi.org/10.1016/j.pbb.2015.11.011
Gerlai R, Lahav M, Guo S, Rosenthal A (2000) Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol Biochem Be 67(4):773–782. https://doi.org/10.1016/S0091-3057(00)00422-6
Gilmour KM, DiBattista JD, Thomas JB (2005) Physiological causes and consequences of social status in salmonid fish. Integr Comp Biol 45(2):263–273. https://doi.org/10.1093/icb/45.2.263
Guo H, Zhang X, Johnsson JI (2017) Effects of size distribution on social interactions and growth of juvenile black rockfish (Sebastes schlegelii). Appl Anim Behav Sci 194l:135–142. https://doi.org/10.1016/j.applanim.2017.05.004.
Haraldstad T, Haugen TO, Kroglund F, Olsen EM, Höglund E (2019) Migratory passage structures at hydropower plants as potential physiological and behavioural selective agents. Roy Soc Open Sci 6(11):190989. https://doi.org/10.1098/rsos.190989
Hellinger J, Jägers P, Spoida K, Weiss LC, Mark MD, Herlitze S (2020) Analysis of the territorial aggressive behavior of the bioluminescent flashlight fish photoblepharon steinitzi in the Red Sea. Front Mar Sci 7:78. https://doi.org/10.3389/fmars.2020.00078
Hirschenhauser K, Wittek M, Johnston P, Möstl E (2008) Social context rather than behavioral output or winning modulates post-conflict testosterone responses in Japanese quail (Coturnix japonica). Physiol Behav 95(3):457–463. https://doi.org/10.1016/j.physbeh.2008.07.013
Hu Y, Liu Y, Zhou C, Li H, Fan J, Ma Z (2021) Effects of food quantity on aggression and monoamine levels of juvenile pufferfish (Takifugu rubripes). Fish Physiol Biochem 47(6):1983–1993. https://doi.org/10.1007/s10695-021-01026-4
Hubená P, Horký P, Slavík O (2020) Test-dependent expression of behavioral syndromes: a study of aggressiveness, activity, and stress of chub. Aggress Behav 46(5):412–424. https://doi.org/10.1002/ab.21909
Huntingford F, Adams C (2005) Behavioural syndromes in farmed fish: implications for production and welfare. Behaviour 1207-1221.https://doi.org/10.1163/156853905774539382
Hvas M, Folkedal O, Oppedal F (2021) Fish welfare in offshore salmon aquaculture. Rev Aquacult 13(2):836–852. https://doi.org/10.1111/raq.12501
Ibabe I (2020) A systematic review of youth-to-parent aggression: conceptualization, typologies, and instruments. Front Psychol 11:577757. https://doi.org/10.3389/fpsyg.2020.577757
Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35(5):1291–1301. https://doi.org/10.1016/j.neubiorev.2011.02.003
Laberge F, Yin-Liao I, Bernier NJ (2019) Temporal profiles of cortisol accumulation and clearance support scale cortisol content as an indicator of chronic stress in fish. Conserv Physiol 7(1):coz052. https://doi.org/10.1093/conphys/coz052
Liu ZH, Li YW, Hu W, Chen QL, Shen YJ (2020) Mechanisms involved in tributyltin-enhanced aggressive behaviors and fear responses in male zebrafish. Aquat Toxicol 220:105408. https://doi.org/10.1016/j.aquatox.2020.105408
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(15):2680–2690. https://doi.org/10.1242/jeb.100685
Lü H, Zhang X, Xi D, Gao T (2014) Use of calcein and alizarin red S for immersion marking of black rockfish Sebastes schlegelii juveniles. Chin J Oceanol Limn 32(1):88–98. https://doi.org/10.1007/s00343-014-3022-9
Ma Z, Li H, Hu Y, Fan J, Liu Y (2021) Growth performance, physiological, and feeding behavior effect of Dicentrarchus labrax under different culture scales. Aquaculture 534:736291. https://doi.org/10.1016/j.aquaculture.2020.736291
Manuel R, Boerrigter JGJ, Cloosterman M, Gorissen M, Flik G, van den Bos R, van de Vis H (2016) Effects of acute stress on aggression and the cortisol response in the A frican sharptooth catfish Clarias gariepinus: differences between day and night. J Fish Biol 88(6):2175–2187. https://doi.org/10.1111/jfb.12989
Marks C, West TN, Bagatto B (2005) Moore FB (2005) Developmental environment alters conditional aggression in zebrafish. Copeia 4:901–908. https://doi.org/10.1643/0045-8511(2005)005[0901:DEACAI]2.0.CO;2
Martínez-Porchas M, Martínez-Córdova LR, Ramos-Enriquez R (2009) Cortisol and glucose: reliable indicators of fish stress?. Pan-Am J Aquat Sci 4(2):158–178. https://www.researchgate.net/publication/237165581.
Metcalfe NB, Van Leeuwen TE, Killen SS (2016) Does individual variation in metabolic phenotype predict fish behaviour and performance? J Fish Biol 88(1):298–321. https://doi.org/10.1111/jfb.12699
Moltesen M, Laursen DC, Thörnqvist PO, Andersson MÅ, Winberg S, Höglund E (2016) Effects of acute and chronic stress on telencephalic neurochemistry and gene expression in rainbow trout (Oncorhynchus mykiss). J Exp Biol 219(24):3907–3914. https://doi.org/10.1242/jeb.139857
Moretz JA, Martins EP, Robison BD (2007) The effects of early and adult social environment on zebrafish (Danio rerio) behavior. Environ Biol Fish 80(1):91–101. https://doi.org/10.1007/s10641-006-9122-4
Moretz JA, Martins EP, Robison BD (2007) Behavioral syndromes and the evolution of correlated behavior in zebrafish. Behav Ecol 18(3):556–562. https://doi.org/10.1093/beheco/arm011
Oliveira RF, Carneiro LA, Canário AV (2005) No hormonal response in tied fights. Nature 437(7056):207–208. https://doi.org/10.1038/437207a
Oliveira RF, Silva JF, Simoes JM (2011) Fighting zebrafish: characterization of aggressive behavior and winner–loser effects. Zebrafish 8(2):73–81. https://doi.org/10.1089/zeb.2011.0690
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. P Natl A Sci 113(5):E654–E661. https://doi.org/10.1073/pnas.1514292113
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 Evolut 54(5):263–275. https://doi.org/10.1159/000006627
Paull GC, Filby AL, Giddins HG, Coe TS, Hamilton PB, Tyler CR (2010) Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. Zebrafish 7(1):109–117. https://doi.org/10.1089/zeb.2009.0618
Qian ZM, Chen YQ (2017) Feature point based 3D tracking of multiple fish from multi-view images. PLoS ONE 12(6):e0180254. https://doi.org/10.1371/journal.pone.0180254
Quadros VA, Costa FV, Canzian J, Nogueira CW, Rosemberg DB (2018) Modulatory role of conspecific alarm substance on aggression and brain monoamine oxidase activity in two zebrafish populations. Prog Neuro-Psychoph 86:322–330. https://doi.org/10.1016/j.pnpbp.2018.03.018
Rault JL, Hintze S, Camerlink I, Yee JR (2020) Positive welfare and the like: distinct views and a proposed framework. Front Vet Sci 7:370. https://doi.org/10.3389/fvets.2020.00370
Sadoul B, Geffroy B (2019) Measuring cortisol, the major stress hormone in fishes. J Fish Biol 94(4):540–555. https://doi.org/10.1111/jfb.13904
Sherman GD, Mehta PH (2020) Stress, cortisol, and social hierarchy. Curr Opin Psychol 33:227–232. https://doi.org/10.1016/j.copsyc.2019.09.013
Sloman KA, Metcalfe NB, Taylor AC, Gilmour KM (2001) Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout. Physiol Biochem Zool 74(3):383–389. https://doi.org/10.1086/320426
Teles MC, Oliveira RF (2016) Quantifying aggressive behavior in zebrafish. In Zebrafish 293–305. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-3771-4_20
Vindas MA, Gorissen M, Höglund E, Flik G, Tronci V, Damsgård B, Thörnqvist PO, Nilsen TO, Winberg S, Øverli Ø, Ebbesson LO (2017a) How do individuals cope with stress? Behavioural, physiological and neuronal differences between proactive and reactive coping styles in fish. J Exp Biol 220(8):1524–1532. https://doi.org/10.1242/jeb.153213
Vindas MA, Magnhagen C, Brännäs E, Øverli Ø, Winberg S, Nilsson J, Backström T (2017b) Brain cortisol receptor expression differs in Arctic charr displaying opposite coping styles. Physiol Behav 177:161–168. https://doi.org/10.1016/j.physbeh.2017.04.024
Way GP, Ruhl N, Snekser JL, Kiesel AL, McRobert SP (2015) A comparison of methodologies to test aggression in zebrafish. Zebrafish 12(2):144–151. https://doi.org/10.1089/zeb.2014.1025
Whittaker BA, Consuegra S, de Leaniz CG (2021) Personality profiling may help select better cleaner fish for sea-lice control in salmon farming. Rev Aquacuture. https://doi.org/10.1101/2021.05.21.444956
Winberg S, Thörnqvist PO (2016) Role of brain serotonin in modulating fish behavior. Curr Zool 62(3):317–323. https://doi.org/10.1093/cz/zow037
Wolkers CPB, Serra M, Barbosa Júnior A, Urbinati EC (2017) Acute fluoxetine treatment increases aggressiveness in juvenile matrinxã (Brycon amazonicus). Fish Physiol Biochem 43(3):755–759. https://doi.org/10.1007/s10695-016-0329-9
Wrangham RW (2018) Two types of aggression in human evolution. P Natl A Sci 115(2):245–253. https://doi.org/10.1073/pnas.1713611115
Xi D, Zhang X, Lü H, Zhang Z (2017) Cannibalism in juvenile black rockfish, Sebastes schlegelii (Hilgendorf, 1880), reared under controlled conditions. Aquaculture 479:682–689. https://doi.org/10.1016/j.aquaculture.2017.07.007
Xi D, Zhang X, Lü H, Zhang Z (2017) Prediction of cannibalism in juvenile black rockfish, Sebastes schlegelii (Hilgendorf, 1880), based on morphometric characteristics and paired trials. Aquac Res 48(6):3198–3206. https://doi.org/10.1111/are.13150
Xu X, Zhang Z, Guo H, Qin J, Zhang X (2020) Changes in aggressive behavior, cortisol and brain monoamines during the formation of social hierarchy in black rockfish (Sebastes schlegelii). Animals 10(12):2357. https://doi.org/10.3390/ani10122357
Yuan M, Chen Y, Huang Y, Lu W (2018) Behavioral and metabolic phenotype indicate personality in zebrafish (Danio rerio). Front Physiol 9:653. https://doi.org/10.3389/fphys.2018.00653
Zabegalov KN, Kolesnikova TO, Khatsko SL, Volgin AD, Yakovlev OA, Amstislavskaya TG, Friend AJ, Bao W, Alekseeva PA, Lakstygal AM, Meshalkina DA, Demin KA, de Abreu MS, Rosemberg DB, Kalueff AV (2019) Understanding zebrafish aggressive behavior. Behav Process 158:200–210. https://doi.org/10.1016/j.beproc.2018.11.010
Zhang Z, Xu X, Wang Y, Zhang X (2020) Effects of environmental enrichment on growth performance, aggressive behavior and stress-induced changes in cortisol release and neurogenesis of black rockfish Sebastes schlegelii. Aquaculture 528:735483. https://doi.org/10.1016/j.aquaculture.2020.735483
Zhang Z, Fu Y, Zhang Z, Zhang X, Chen S (2021) A comparative study on two territorial fishes: the influence of physical enrichment on aggressive behavior. Animals 11(7):1868. https://doi.org/10.3390/ani11071868
Zhu W, Zhou X, Xia LX (2019) Brain structures and functional connectivity associated with individual differences in trait proactive aggression. Sci Rep 9(1):1–12. https://doi.org/10.1038/s41598-019-44115-4
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This work was supported by the National Natural Science Foundation of China (32102753; 42030408), the Scientific and Technical Innovation Project of Dalian, Liaoning Province, China (2021JJ13SN72), and by contributions from the AET. Special thanks are also given to the anonymous reviewers for their constructive comments regarding the manuscript.
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Haixia Li: conceptualization, methodology, investigation, and writing-original draft. Zhen Ma: conceptualization, resources, writing-original draft, writing-review & editing, supervision, and funding acquisition. Jie Wang: methodology and investigation. Xu Zhang: methodology and investigation. Yu Hu: methodology and investigation. Ying Liu: conceptualization, resources, and funding acquisition.
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Li, H., Wang, J., Zhang, X. et al. Comparing behavioral performance and physiological responses of Sebastes schlegelii with different aggressiveness. Fish Physiol Biochem 48, 1333–1347 (2022). https://doi.org/10.1007/s10695-022-01123-y
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DOI: https://doi.org/10.1007/s10695-022-01123-y