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Locomotor kinematics and behaviour in the escape response of European sea bass, Dicentrarchus labrax L., exposed to hypoxia

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Abstract

To assess the effect of oxygen reduction on the escape response of sea bass, Dicentrarchus labrax, an integrative experimental approach was employed. The effect of hypoxia was tested on locomotor variables, i.e. cumulative distance (D), maximum swimming speed (V max) and maximum acceleration (A max). Behavioural variables, such as responsiveness (i.e. the proportion of individuals responding out of the total number of fish tested), response latency (i.e. the time interval between stimulus onset and the first detectable movement leading to the escape of the animal) and directionality (i.e. the proportion of escape responses in which the first detectable movement of the head was oriented away or towards the stimulus at its onset) were also considered. Four levels of oxygen were used: >85% (i.e. normoxia, the control treatment), 50, 20 and 10% of air saturation. Sea bass responsiveness decreased significantly at 10% of air saturation, while hypoxia did not have any effect on the response latency. At the onset of the escape response, the proportion of away/towards responses was random when oxygen was ≤50% of air saturation, suggesting an impairment of the left–right discrimination. Whatever the level of hypoxia, none of the locomotor variables (i.e. D, V max and A max) was significantly different from normoxia. Our study suggests that hypoxia may reduce sea bass elusiveness facing a predator by directly affecting its escape behaviour, possibly related to an impairment of the mechano-sensory performance and/or in the Mauthner cells involved in triggering the escape response.

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Reference

  • Addis P, Cau A (1997) Impact of the feeding habits of the great cormorant Phalacrocorax carbo sinensis on the lagoon fish-stocks in central-western Sardinia. Avocetta 21:180–187

    Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic Press, NewYork

    Google Scholar 

  • Batty RS (1989) Escape responses of herring larvae to visual stimuli. J Mar Biol Assoc UK 69:647–654

    Google Scholar 

  • Beamish FWH (1978) Swimming capacity. In: Hoar WS, Randall DJ (eds) Fish physiology, VII. Academic press, NY, S. Francisco, London, pp 101–187

    Google Scholar 

  • Blaxter JHS, Batty RS (1987) Comparisons of herring behaviour in the light and dark: changes in activity and responses to sound. J Mar Biol Assoc UK 67:849–860

    Article  Google Scholar 

  • Breitburg DL, Steinberg N, DuBeau S, Cooksey C, Houde ED (1994) Effects of low dissolved oxygen on predation on estuarine fish larvae. Mar Ecol Prog Se. 104:235–246

    Article  Google Scholar 

  • Breitburg DL, Adamack A, Rose KA, Kolesar SE, Decker MB, Purcell JE, Keister JE, Cowan JH (2003) The pattern and influence of low dissolver oxygen in the Patuxent River, a seasonally hypoxic estuary. Estuaries 26(2A):280–297

    CAS  Google Scholar 

  • Bushnell PG, Steffensen JF, Johansen K (1984) Oxygen consumption and swimming performance in hypoxia-acclimated rainbow trout Salmo gairdneri. J Exp Biol 113:225–235

    Google Scholar 

  • Canfield JG, Eaton RC (1990) Swimbladder acoustic pressure transduction initiates Mauthner-mediated escape. Nature 347:760–762

    Article  Google Scholar 

  • Canfield JG, Rose GJ (1996) Hierarchical sensory guidance of Mauthner-mediated escape responses in Goldfish (Carassius auratus) and Cichlids (Haplochromis burtoni). Brain Behav Evol 48:137–156

    PubMed  CAS  Google Scholar 

  • Cech JJ, Mitchell SJ, Castleberry DT, McEnroe M (1990) Distribution of California stream fishes: influence of environmental temperature and hypoxia. Environ Biol Fish 29:95–105

    Article  Google Scholar 

  • Chabot D, Dutil JD (1999) Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J Fish Biol 55:472–491

    Article  Google Scholar 

  • Chapman LJ, Galis F, Shinn J (2000) Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid. Ecol lett 3:387–393

    Article  Google Scholar 

  • Claireaux G, Lagardère JP (1999) Influence of temperature, oxygen and salinity on the metabolism of European sea bass. J Sea Res 42:157–168

    Article  CAS  Google Scholar 

  • D’amours D (1993) The distribution of cod (Gadus morhua) in relation to temperature and oxygen level in the Gulf of St Lawrence. Fisheries Oceanogr 2:24–29

    Google Scholar 

  • Dean TL, Richardson J (1999) Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen. New Zeal J Mar Fresh 33(1):99–106

    Article  Google Scholar 

  • Domenici P (2002a) The visually-mediated escape response in fish: Predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar Freshw Behav Phy 35:87–110

    Article  Google Scholar 

  • Domenici P (2002b) Escape trajectory, ecological. In: El-Shaarawi AH, Piegorsch WW (eds) Encyclopedia of Environmetrics. J Wiley and Sons, Chichester, pp 708–711

    Google Scholar 

  • Domenici P, Batty RS (1997) Escape behaviour of solitary herring (Clupea harengus) and comparisons with schooling individuals. Mar Biol 128:29–38

    Article  Google Scholar 

  • Domenici P, Blake RW (1991) The kinematics and performance of the escape response in the angelfish (Pterophyllum eimekei). J Exp Biol 156:187–205

    Google Scholar 

  • Domenici P, Blake RW (1993a) Escape trajectories in angelfish (Pterophyllum eimekei). J Exp Biol 177:253–272

    Google Scholar 

  • Domenici P, Blake RW (1993b) The effect of size on the kinematics and performance of angelfish (Pterophyllum eimekei) escape responses. Can J Zool 71:2319–2326

    Article  Google Scholar 

  • Domenici P, Blake RW (1997) Fish fast start kinematics and performance. J Exp Biol 200(8):1165–1178

    PubMed  Google Scholar 

  • Domenici P, Standen EM, Levine RP (2004) Escape manoeuvres in the spiny dogfish (Squalus acanthilas). J Exp Biol 207(13):2339–2349

    Article  PubMed  Google Scholar 

  • Domenici P, Steffensen JF, Batty RS (2000) The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring. J Fish Biol 57:1526–1538

    Article  Google Scholar 

  • Domenici P, Ferrari RS, Steffensen JF, Batty RS (2002) The effects of progressive hypoxia on school structure and dynamics in Atlantic herring Clupea harengus. Proc R Soc Lond B 269:2103–2111

    Article  Google Scholar 

  • Druon JN, Schrimpff W, Dobricic S, Stips A (2004) Comparative assessment of large-scale marine eutrophication: North Sea area and Adriatic Sea as case studies. Mar Ecol Prog Ser 272:1–23

    Google Scholar 

  • Eaton RC, Nissanov J, Wieland CM (1984) Differential activation of Mauthner and non-Mauthner startle circuits in the Zebrafish-implications for functional substitutions. J Comp Physiol 155:813–820

    Article  Google Scholar 

  • Foreman MB, Eaton RC (1993) The direction change concept for reticulospinal control of goldfish escape. J Neurosci 13:4101–4133

    PubMed  CAS  Google Scholar 

  • Fritsche R, Nilsson S (1989) Cardiovascular responses to hypoxia in the Atlantic cod, Gadus morhua. J Exp Biol 48:153–160

    CAS  Google Scholar 

  • Fry FE (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish physiology, VI. Academic press, NY, S.Francisco, London, pp 1–98

    Google Scholar 

  • Harper DG, Blake RW (1991) Prey capture and the faststart performance of northern pike Esox lucius. J Exp Biol 155:175–192

    Google Scholar 

  • Jayne BC, Lauder GV (1993) Red and white muscle activity and kinematics of the escape response of the bluegill sunfish during swimming. J Comp Physiol A 173:495–508

    Article  Google Scholar 

  • Lanczos C (1956). Applied Analysis. Prentice Hall, Eaglewood Cliffs, NJ

    Google Scholar 

  • Lefrançois C, Claireaux G (2003) Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate of the sole (Solea solea). Mar Ecol Prog Ser 259:273–284

    Google Scholar 

  • Lefrançois C, Shingles A, Domenici P (2005) The effect of hypoxia on locomotor performance and behaviour during escape in the golden grey mullet (Liza aurata). J Fish Biol 67:1711–1729

    Article  Google Scholar 

  • McFarland WN, Klontz GW (1969) Anaesthesia in fishes. Federation Proceedings 28(4):1535–1540

    PubMed  CAS  Google Scholar 

  • McKinsey DM, Chapman LJ (1998) Dissolved oxygen and fish distribution in a Florida spring. Environ Biol Fish 53:211–223

    Article  Google Scholar 

  • Petersen JK, Pihl L (1995) Responses to hypoxia of plaice, Pleuronectes platessa, and dab, Limanda limanda, in the south-east Kattegat: distribution and growth. Environ Biol Fish 43:311–321

    Article  Google Scholar 

  • Pichavant K, Person-Le-Ruyet J, Le Bayon N, Sévère A, Le Roux A, Quémerer L, Maxime V, Nonotte G, Bœuf G (2000) Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 188:103–104

    Article  Google Scholar 

  • Plante S,Chabot D, Dutil JD (1998) Hypoxia tolerance in Atlantic cod. J Fish Biol 53:1342–1356

    Article  Google Scholar 

  • Preuss T, Faber DS (2003) Central cellular mechanisms underlying temperature-dependent changes in the goldfish startle escape behaviour. J Neurosci 23(13):5617–5626

    PubMed  CAS  Google Scholar 

  • Priede IG (1985) Metabolic scope in fishes. In: Tytler P, Calow P (eds) Fish energetics: new perspectives. Croom Helm, London, Sydney. pp 33–64

    Google Scholar 

  • Quero JC, Vayne JJ (2005) Les poisons de mer des pêches françaises, Delachaux and Niestlé, Lausanne, Paris

  • Randall D (1982) The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100:275–288

    Google Scholar 

  • Rydberg L, Edler L, Floderus S, Granéli W (1990) Interaction between supply of nutrients, primary production, sediment and oxygen consumption in SE Kattegat. Ambio 19:134–141

    Google Scholar 

  • Satchell GH (1971) Physiology and form of fish circulation. Cambridge University Press, Cambridge, New York, Port Chester, Melbourne, Sydney

    Google Scholar 

  • Sitko S, Honrubia V (1986) Differential effects of ischemia on spontaneous and sinusoidal-evoked activity in the semicircular canal afferents in the bullfrog. Acta Otolaryngol 102:179–185

    PubMed  CAS  Google Scholar 

  • Shellart NAM, Wubbels RJ (1998) The auditory and mechanosensory lateral line system. In: Evans DH (eds) The physiology of fishes. CRC Marine Sciences Series, Florida, pp 283–312

    Google Scholar 

  • Shingles A, McKenzie DJ, Claireaux G, Domenici P (2005) Reflex cardioventilatory responses to hypoxia in the flathead grey mullet (Mugil cephalus) and their behavioural modulation by perceived threat of predation and water turbidity. Physiol Biochem Zool 78:744–755

    Article  PubMed  CAS  Google Scholar 

  • Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673

    Article  PubMed  Google Scholar 

  • Steffensen JF, Farrell A (1998) Swimming performance, venous oxygen tension and cardiac performance of coronary-ligated rainbow trout, Oncorhynchus mykiss, exposed to progressive hypoxia. Comp Biochem Physiol 119A(2):585–592

    CAS  Google Scholar 

  • Thetmeyer H, Waller U, Black KD, Inselmann S, Posenthal H (1999) Growth of European sea bass (Dicentrarchus labrax L.) under hypoxic and oscillating oxygen conditions. Aquaculture 174(3–4):355–367

    Article  Google Scholar 

  • Wakeling JM, Johnston IA (1998) Muscle power output limits fast-start performance in fish. J Exp Biol 201:1505–1526

    PubMed  CAS  Google Scholar 

  • Webb PW (1976) The effect of size on the fast-start performance of rainbow trout Salmo gairdneri and a consideration of piscivorous predator-prey interaction. J Exp Biol 65:157–177

    PubMed  CAS  Google Scholar 

  • Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120

    Google Scholar 

  • Webb PW (1988) Steady swimming kinematics of tiger musky, an esociform accelerator, and Rainbow trout, a generalist cruiser. J Exp Biol 138:51–69

    Google Scholar 

  • Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Marine-pollution-bulletin. 45(1–12):35–45

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, New Jersey

    Google Scholar 

  • Zottoli SJ, Hordes AR, Faber DS (1987) Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Res 401:113–121

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work is part of a post-doctoral fellowship awarded to CL by the Commission of the European Communities (qlk5-ct-2001-500977). financial support by the Italian MIUR (project STM) is acknowledged. The authors would like also to thank Aimée Bouquet for her active participation to the experiments. All experimental procedures in this work comply with the current regulations in Italy (n°116/1992).

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Correspondence to C. Lefrançois.

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Communicated by S.A. Poulet, Roscoff

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Lefrançois, C., Domenici, P. Locomotor kinematics and behaviour in the escape response of European sea bass, Dicentrarchus labrax L., exposed to hypoxia. Mar Biol 149, 969–977 (2006). https://doi.org/10.1007/s00227-006-0261-0

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