Behavioural Monitoring Underlines Habituation to Repeated Stressor Stimuli in Farmed Gilthead Sea Bream () Reared at a High Stocking Density

Overview

Journal Biology (Basel)

Publisher MDPI

Specialty Biology

Date 2024 Nov 27

PMID 39596834

Authors

Paul G Holhorea

Fernando Naya-Catala

Ricardo Domingo-Breton

Federico Moroni

Alvaro Belenguer

Josep A Calduch-Giner

Jaume Perez-Sanchez

Affiliations

Soon will be listed here.

Abstract

A confinement stress test with 75% tank space reduction and behavioural monitoring through tri-axial accelerometers externally attached to the operculum was designed. This procedure was validated by demonstrating the less pronounced stress response in gilthead sea bream than in European sea bass (950-1200 g). Our study aimed to assess habituation to high stocking densities with such procedure in gilthead sea bream. Animals (420-450 g) were reared (June-August) in a flow-through system at two stocking densities (CTRL: 10-15 kg/m; HD: 18-24 kg/m), with natural photoperiod and temperature (21-29 °C), and oxygen levels at 5.2-4.2 (CTRL) and 4.2-3.2 ppm (HD). At the end, blood and muscle were sampled for haematology and transcriptomic analyses, and external tissue damage was assessed by image-based scoring. Four days later, fish underwent a 45 min confinement stress test over two consecutive days. HD fish showed reduced feed intake, growth rates and haematopoietic activity. Muscle transcriptome changes indicated a shift from systemic to local growth regulation and a primed muscle regeneration over protein accretion in HD animals with slight external injuries. After stress testing, HD fish exhibited a decreased recovery time in activity and respiration rates, which was shorter after a second stressor exposure, confirming habituation to high densities.

References

Barton B . Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol. 2011; 42(3):517-25. DOI: 10.1093/icb/42.3.517. View

Wang Z, Pu D, Zheng J, Li P, Lu H, Wei X . Hypoxia-induced physiological responses in fish: From organism to tissue to molecular levels. Ecotoxicol Environ Saf. 2024; 267:115609. DOI: 10.1016/j.ecoenv.2023.115609. View

Romagnoli C, Iantomasi T, Brandi M . Available In Vitro Models for Human Satellite Cells from Skeletal Muscle. Int J Mol Sci. 2021; 22(24). PMC: 8706222. DOI: 10.3390/ijms222413221. View

Farhat E, Cheng H, Romestaing C, Pamenter M, Weber J . Goldfish Response to Chronic Hypoxia: Mitochondrial Respiration, Fuel Preference and Energy Metabolism. Metabolites. 2021; 11(3). PMC: 8004290. DOI: 10.3390/metabo11030187. View

Fernandes-de-Castilho M, Pottinger T, Volpato G . Chronic social stress in rainbow trout: does it promote physiological habituation?. Gen Comp Endocrinol. 2007; 155(1):141-7. DOI: 10.1016/j.ygcen.2007.04.008. View

Zammit P . Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Semin Cell Dev Biol. 2017; 72:19-32. DOI: 10.1016/j.semcdb.2017.11.011. View

McFarland D, Velleman S, Pesall J, Liu C . Effect of myostatin on turkey myogenic satellite cells and embryonic myoblasts. Comp Biochem Physiol A Mol Integr Physiol. 2006; 144(4):501-8. DOI: 10.1016/j.cbpa.2006.04.020. View

Arechavala-Lopez P, Nazzaro-Alvarez J, Jardi-Pons A, Reig L, Carella F, Carrasson M . Linking stocking densities and feeding strategies with social and individual stress responses on gilthead seabream (Sparus aurata). Physiol Behav. 2019; 213:112723. DOI: 10.1016/j.physbeh.2019.112723. View

Naya-Catala F, Martos-Sitcha J, de Las Heras V, Simo-Mirabet P, Calduch-Giner J, Perez-Sanchez J . Targeting the Mild-Hypoxia Driving Force for Metabolic and Muscle Transcriptional Reprogramming of Gilthead Sea Bream () Juveniles. Biology (Basel). 2021; 10(5). PMC: 8151949. DOI: 10.3390/biology10050416. View

10.

Herman J . Neural control of chronic stress adaptation. Front Behav Neurosci. 2013; 7:61. PMC: 3737713. DOI: 10.3389/fnbeh.2013.00061. View

11.

Sharma M, Langley B, Bass J, Kambadur R . Myostatin in muscle growth and repair. Exerc Sport Sci Rev. 2001; 29(4):155-8. DOI: 10.1097/00003677-200110000-00004. View

12.

Jia R, Liu B, Feng W, Han C, Huang B, Lei J . Stress and immune responses in skin of turbot (Scophthalmus maximus) under different stocking densities. Fish Shellfish Immunol. 2016; 55:131-9. DOI: 10.1016/j.fsi.2016.05.032. View

13.

Gesto M . Consistent individual competitive ability in rainbow trout as a proxy for coping style and its lack of correlation with cortisol responsiveness upon acute stress. Physiol Behav. 2019; 208:112576. DOI: 10.1016/j.physbeh.2019.112576. View

14.

Winberg S, Sneddon L . Impact of intraspecific variation in teleost fishes: aggression, dominance status and stress physiology. J Exp Biol. 2022; 225(20). DOI: 10.1242/jeb.169250. View

15.

Gorr T . Hypometabolism as the ultimate defence in stress response: how the comparative approach helps understanding of medically relevant questions. Acta Physiol (Oxf). 2016; 219(2):409-440. DOI: 10.1111/apha.12747. View

16.

Jesus J, Amorim M, Fonseca P, Teixeira A, Natario S, Carrola J . Acoustic barriers as an acoustic deterrent for native potamodromous migratory fish species. J Fish Biol. 2018; 95(1):247-255. DOI: 10.1111/jfb.13769. View

17.

Sangiao-Alvarellos S, Guzman J, Laiz-Carrion R, Miguez J, Martin Del Rio M, Mancera J . Interactive effects of high stocking density and food deprivation on carbohydrate metabolism in several tissues of gilthead sea bream Sparus auratus. J Exp Zool A Comp Exp Biol. 2005; 303(9):761-75. DOI: 10.1002/jez.a.203. View

18.

Brown C . Fish intelligence, sentience and ethics. Anim Cogn. 2014; 18(1):1-17. DOI: 10.1007/s10071-014-0761-0. View

19.

Toxqui-Rodriguez S, Holhorea P, Naya-Catala F, Calduch-Giner J, Sitja-Bobadilla A, Piazzon C . Differential Reshaping of Skin and Intestinal Microbiota by Stocking Density and Oxygen Availability in Farmed Gilthead Sea Bream (): A Behavioral and Network-Based Integrative Approach. Microorganisms. 2024; 12(7). PMC: 11278760. DOI: 10.3390/microorganisms12071360. View

20.

Hernandez-Hernandez J, Garcia-Gonzalez E, Brun C, Rudnicki M . The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration. Semin Cell Dev Biol. 2017; 72:10-18. PMC: 5723221. DOI: 10.1016/j.semcdb.2017.11.010. View