Abstract
In fish, defensive reactions are induced by different chemical cues that emanate from sense-related stresses [physical, chemical, and visual (visual contact with predator)] or food stresses (acute fasting and chronic food restriction). Using a shuttle box with a two-chamber unmixed laminar flow that allowed fish to remain or flee from a chemical cue, we showed that the avoidance response depended on the type of the chemical cue. We show that zebrafish (Danio rerio) retreated from water conditioned with chemical cues released by chemically or physically stressed fish and acutely fasted fish, but not from water with cues from fish experiencing visual contact with predatory fish or fish suffering from chronic food restriction. Our data reinforced the hypothesis that fish use a combination of information and the context of the situation to determine their evasion strategy.
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References
Abreu MS, Giacomini AC, Gusso D, Rosa JG, Koakoski G et al (2016) Acute exposure to waterborne psychoactive drugs attract zebrafish. Comp Biochem Physiol C Toxicol Pharmacol 179:37–43
Alsop D, Vijayan M (2009) The zebrafish stress axis: molecular fallout from the teleost specific genome duplication event. Gen Comp Endocrinol 161:62–66
Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S et al (2000) The synthetic relationship of the zebrafish and human genomes. Genome Res 10:1351–1358
Barcellos LJG, Marqueze A, Trapp M, Quevedo RM, Ferreira D (2010) The effects of fasting on cortisol, blood glucose and liver and muscle glycogen in adult jundiá Rhamdia quelen. Aquaculture 300:231–236
Barcellos LJG, Volpato GL, Barreto RE, Coldebella I, Ferreira D (2011) Chemical communication of handling stress in fish. Phys Behav 103:372–375
Barcellos LJG, Koakoski G, da Rosa JGS, Ferreira D, Barreto RE, Giaquinto PC, Volpato GL (2014) Chemical communication of predation risk in zebrafish does not depend on cortisol increase. Sci Rep 4:5076
Barreto RE, Barbosa A, Giassi ACC, Hoffmann A (2010) The ‘club’ cell and behavioural and physiological responses to chemical alarm cues in the Nile tilapia. Mar Fresh Behav Physiol 43:75–81
Barreto RE, Barbosa-Junior A, Hoffmann A (2012) Ventilatory responses to skin extract in catfish. Aquatic Biol 15:205–214
Baumgarner BL, Cooper BR (2012) Evaluation of a tandem gas chromatography/time-of-flight mass spectrometry metabolomics platform as a single method to investigate the effect of starvation on whole-animal metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 215:1627–1632
Brown C, Braithwaite VA (2005) Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi. Behav Ecol 16:482–487
Burrows MT (1994) An optimal foraging and migration model for juvenile plaice. Evol Ecol 8:125–149
Burrows MT, Gibson RN (1995) The effects of food, predation risk and endogenous rhythmicity on the behaviour of juvenile plaice, Pleuronectes platessaL. Anim Behav 50:41–52
Chivers DP, Smith JF (1998) Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352
Egan R, Bergner CL, Hart PC, Cachat JM et al (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205:38–44
Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–505
Hussain A, Saraiva LR, Ferrero DM, Ahuja G, Krishna VS, Liberles SD, Korsching SI (2013) High-affinity olfactory receptor for the death-associated odor cadaverine. Proc Natl Acad Sci 110:19579–19584
Jayaram MG, Beamish FWH (1992) Influence of dietary protein and lipid on nitrogen and energy losses in lake trout, Salvelinus namaycush. Can J Fish Aquat Sci 49:2267–2272
Jordão LC, Volpato GL (2000) Chemical transfer of warning information in non-injured fish. Behavior 137:681–690
Korpi NL, Wisenden BD (2001) Learned recognition of novel predator odour by zebra danio, Danio rerio, following time-shifted presentation of alarm cue and predator odour. Environ Biol Fishes 61:205–211
Lauff RF, Wood CM (1996) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during starvation in juvenile rainbow trout, Oncorhynchus mykiss. J Comp Physiol B 165:542–551
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Malandrakis EE, Dadali O, Golomazou E, Kavouras M, Dailianis S, Chadio S, Exadactylos A, Panagiotaki P (2016) DNA damage and differential gene expression associated with physical stress in gilthead seabream (Sparus aurata). Gen Comp Endocrinol 236:98–104
McCormick MI, Larson JK (2008) Effect of hunger on the response to, and the production of, chemical alarm cues in a coral reef fish. Anim Behav 75:1973–1980
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9:211–268
Mueller T, Vernier P, Wullimann MF (2004) The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res 1011:156–169
Oliveira TA, Koakoski G, Kreutz LC, Ferreira D, da Rosa JGS et al (2013) Alcohol impairs predation risk response and communication in zebrafish. PLoS One 8:e75780
Pelkowski SD, Kapoor M, Richendrfer HA, Wang X, Colwill RM et al (2011) A novel high-throughput imaging system for automated analyses of avoidance behavior in zebrafish larvae. Behav Brain Res 223:135–144
Pfeiffer W, Lamour D (1976) Effect of alarm substance on the heart rate in Phoxinus phoxinus (L.) (Cyprinidae, Ostariophysi, Pisces). Rev Suisse Zool 83:861–873
Pujante IM, Martos-Sitcha JA, Moyano FJ, Ruiz-Jarabo I, Martínez-Rodríguez G, Mancera JM (2015) Starving/re-feeding processes induce metabolic modifications in thick-lipped grey mullet (Chelon labrosus, Risso 1827). Comp Biochem Physiol B 180:57–67
Readman GD, Owen SF, Murrell TG (2013) Knowles. Do fish perceive anaesthetics as aversive? PLoS ONE 8:e73773
Rehnberg BG, Schreck CB (1987) Chemosensory detection of predators by coho salmon (Oncorhynchus kisutch)—behavioral reaction and the physiological stress response. Can J Zool 65:481–485
Rehnberg BG, Smith RJF, Sloley BD (1987) The reaction of pearl dace (Pisces, Cyprinidae) to alarm substance time-course of behavior, brain amines, and stress physiology. Can J Zool 65:2916–2921
Rossi A, Cazenave J, Bacchetta C, Campana M, Parma MJ (2015) Physiological and metabolic adjustments of Hoplosternum littorale (Teleostei, Callichthyidae) during starvation. Ecol Indic 56:161–170
Sabet SS, Neo YY, Slabbekoorn H (2015) The effect of temporal variation in sound exposure on swimming and foraging behaviour of captive zebrafish. Anim Behav 107:49–60
Sanches FHC, Miyai CA, Pinho-Neto CF, Barreto RE (2015) Stress responses to chemical alarm cues in Nile tilapia. Physiol Behav 149:8–13
Schwarze S, Bleckmann H, Schluessel V (2013) Avoidance conditioning in bamboo sharks (Chiloscyllium griseum and C. punctatum): behavioral and neuroanatomical aspects. J Comp Physiol A 199:843–856
Toa DG, Afonso LOB, Iwama GK (2004) Stress response of juvenile rainbow trout (Oncorhynchus mykiss) to chemical cues released from stressed conspecifics. Fish Physiol Biochem 30:103–108
Trudeau VL, Martyniuk CJ, Zhao E, Hu H, Volkoff H, Decatur WA, Basak A (2012) Is secretoneurin a new hormone? Gen Comp Endocrinol 175:10–18
Turner JW, Nemeth R, Rogers C (2003) Measurement of fecal glucocorticoids in parrot fishes to assess stress. Gen Comp Endocrinol 133:341–352
Vermeirssen ELM, Scott AP (1996) Excretion of free and conjugated steroids in rainbow trout (Oncorhynchus mykiss): evidence for branchial excretion of the maturation-inducing steroid, 17,20b-dihydroxy-4-pregnen-3-one. Gen Comp Endocrinol 101:180–194
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625
Wilkie MP (2002) Ammonia excretion and urea handling by fish gills: present understanding and future research challenges. J Exp Zool 293:284–301
Acknowledgments
This study was approved by the Ethics Committee on Animal Use (CEUA) of the University of Passo Fundo (UPF), registration 29/2014, meeting the guidelines of the National Council of Animal Experimentation Control (CONCEA). The study was funded by the Universidade de Passo Fundo, and CNPq L.J.G.B. and R.E.B. hold CNPq research fellowships (301992/2014-2 and 302719/2013-0, respectively). ANYmaze® software (Stoelting, Co, USA) provided this software for behavioral analysis. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Abreu, M.S., Giacomini, A.C.V., Gusso, D. et al. Behavioral responses of zebrafish depend on the type of threatening chemical cues. J Comp Physiol A 202, 895–901 (2016). https://doi.org/10.1007/s00359-016-1129-5
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DOI: https://doi.org/10.1007/s00359-016-1129-5