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Impact of a plant-based diet on behavioural and physiologicaltraits in sea bass (Dicentrarchus labrax)

Published online by Cambridge University Press:  12 April 2013

David Benhaïm ,
Marie-Laure Bégout ,
Samuel Péan ,
Michaël Manca ,
Patrick Prunet  and
Béatrice Chatain
David Benhaïm*
Affiliation:
LERMA, INTECHMER/CNAM, BP 324, 50103 Cherbourg Cedex, France
Marie-Laure Bégout
Affiliation:
Ifremer, Laboratoire Ressources halieutiques, place Gaby Coll, BP 7, 17137 L'Houmeau, France
Samuel Péan
Affiliation:
Ifremer, Laboratoire Ressources halieutiques, place Gaby Coll, BP 7, 17137 L'Houmeau, France
Michaël Manca
Affiliation:
Ifremer, Laboratoire Ressources halieutiques, place Gaby Coll, BP 7, 17137 L'Houmeau, France
Patrick Prunet
Affiliation:
INRA-SCRIBE, Fish Biology of Stress and Adaptation Group, 35042 Rennes Cedex, France
Béatrice Chatain
Affiliation:
Station expérimentale d’aquaculture, Ifremer, Laboratoire de recherche piscicole de Méditerranée, Chemin de Maguelone, 34250 Palavas-Les-Flots, France
*
a Corresponding author: [email protected]
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Abstract

Replacing aquaculture feeds based on fisheries-derived resources with plant-based dietscould be a relevant strategy to improve the sustainability of aquaculture. Recent studieson sea bass have shown that the total and early replacement of marine products by plantproducts would have a moderate effect on fish growth and body lipid content. Whether aplant-based diet impacts behavioural and physiological traits possibly linked to fishwelfare, is not known, however. Here, we studied the effect of a totally plant-based dietintroduced at an early stage of sea bass development on self-feeding behaviour, learningability in a T-maze and stress biomarkers. We first compared learning processes inself-feeding conditions, between naive fish fed a plant-based diet (PBF) and fish fed aclassic marine diet (MF). Then, we tested fish individually in a T-maze to compare the twofeed groups for swimming activity, exploration and the ability to learn to discriminatebetween two two-dimensional objects associated with a reward. Blood physiologicalvariables, including stress indicators (cortisol and glucose concentrations), were alsodetermined. We did not find any indications of differences in self-feeding behaviourbetween PBF and MF in the first 30 days. A second experiment showed similar swimmingactivities in both fish categories. The “no-choice” percentage was high in both fishcategories (~60%), but all the fish moved preferentially toward the reward. Theirfirst turns indicated an ability to discriminate between two two-dimensional objects tocomplete a simple task. However, the high percentage of “no-choice” responses in both fishcategories could have rendered the results non significant. The T-maze test procedureinduced the production of high concentrations of cortisol, indicating acute stress in fishof both groups during testing. Plasma cortisol concentration was higher in MF than PBF,suggesting that the plant-based diet may affect the short-term release of cortisol. Thisstudy provides the first insight into the impact of a plant-based diet on sea bassbehavioural traits, and confirms the effect of this diet on cortisol release in responseto stress. Overall, in this first experiment, we did not find any major impact of aplant-based diet on sea bass behavioural traits, which is an interesting point for thedevelopment potential of such a sustainable aquaculture strategy.

Keywords

Self-feederPlant-based dietLearningExploratory behaviourCortisolDicentrarchus labrax
Type
Research Article
Information
Aquatic Living Resources , Volume 26 , Issue 2 , April 2013 , pp. 121 - 131
Copyright
© EDP Sciences, IFREMER, IRD 2013

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References

Allen, P.J., Barth, C.C., Peake, S.J., Abrahams, M.V., Anderson, W.G., 2009, Cohesive social behaviour shortens the stress response: the effects of conspecifics on the stress response in lake sturgeon Acipenser fulvescens. J. Fish Biol. 74, 90–104. CrossRefGoogle ScholarPubMed
Alves, C., Chichery, R., Boal, J.G., Dickel, L., 2007, Orientation in the cuttlefish Sepia officinalis: response versus place learning. Anim. Cogn. 10, 29–36. CrossRefGoogle ScholarPubMed
Anthouard, M., Divanach, P., Kentouri, M., 1993, An analysis of feeding activities of sea bass Dicentrarchus labrax, Moronidae raised under different lighting conditions. Ichthyophysiol. Acta 16, 59–70. Google Scholar
Arzel, J., Martinez Lopez, F.X., Métailler, R., Stéphan, G., Viau, M., Gandemer, G., Guillaume, J., 1994, Effect of dietary lipid on growth performance and body composition of brown trout (Salmo trutta) reared in seawater. Aquaculture 123, 361–375. CrossRefGoogle Scholar
Auperin, B., Baroiller, J.-F., Ricordel, J.F., Fostier, A., Prunet, P., 1997, Effect of confinement stress on circulating levels of growth hormone and two prolactins in freshwater-adapted tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 108, 35–44. CrossRefGoogle Scholar
Baroiller, J.F., Guiguen, Y. A.F., 1999, Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 55, 910–931. CrossRefGoogle Scholar
Barton, B.A., 2000, Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N. Am. J. Aquac. 62, 12–18. 2.0.CO;2>CrossRefGoogle Scholar
Benhaïm D., Bégout M.-L., Chatain B., 2013, Unfamiliar congener used as a visual attractor in wild caught and domesticated sea bass (Dicentrarchus labrax) placed in a T-maze. J. Aquac. Res. Develop. doi: 10.4172/2155-9546.1000169
Benítez-Santana, T., Masuda, R., Carrillo, E.J., Ganuza, E., Valencia, A., Hernández-Cruz, C.M., Izquierdo, M.S., 2007, Dietary n-3 HUFA deficiency induces a reduced visual response in gilthead seabream Sparus aurata larvae. Aquaculture 264, 408–417. CrossRefGoogle Scholar
Brown, C., Laland, K., 2001, Social learning and life skills training for hatchery reared fish. J. Fish Biol. 59, 471–493. CrossRefGoogle Scholar
Brown C., Laland K., Krause J., 2007, Fish Cognition and Behaviour. Blackwell Publishing Ltd. Fish Cognition and Behavior.
Cerdá-Reverter, J.M., Zanuy, S., Carrillo, M., Madrid, J.A., 1998, Time-course studies on plasma glucose, insulin and cortisol in Sea Bass (Dicentrarchus labrax) held under different photoperiodic regimes. Physiol. Behav. 64, 245–250. CrossRefGoogle ScholarPubMed
Coeurdacier, J.L., Pepin, J.F., Fauvel, C., Legall, P., Bourmaud, A.F., Romestand, B., 1997, Alterations in total protein, IgM and specific antibody activity of male and female sea bass (Dicentrarchus labrax L., 1758) sera following injection with killed Vibrio anguillarum. Fish Shellfish Immunol. 7, 151–160. CrossRefGoogle Scholar
Covès, D., Beauchaud, M., Attia, J., Dutto, G., Bouchut, C., Bégout, M.L., 2006, Long-term monitoring of individual fish triggering activity on a self-feeding system: An example using European sea bass (Dicentrarchus labrax). Aquaculture 253, 385–392. CrossRefGoogle Scholar
Covès, D., Gasset, E., Lemarié, G., Dutto, G., 1998, A simple way of avoiding feed wastage in European seabass, Dicentrarchus labrax, under self-feeding conditions. Aquat. Living Resour. 11, 395–401. CrossRefGoogle Scholar
Dagnélie P., 1975, Théorie et méthodes statistiques. Applications agronomiques vol. 2. Presses Agronomiques de Gembloux, Gembloux.
Di-Poï C., 2008, Déterminisme de la structure sociale chez le bar juvénile Dicentrarchus labrax en conditions d’auto-nourrissage: Approches neuro-éthologique et physiologique. Thèse dr., Saint-Etienne.
Di Marco, P., Priori, A., Finoia, M.G., Massari, A., Mandich, A., Marino, G., 2008, Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquaculture 275, 319–328. CrossRefGoogle Scholar
Dias, J., Conceicao, L.E.C., Ribeiro, A.R., Borges, P., Valente, L.M.P., Dinis, M.T., 2009, Practical diet with low fish-derived protein is able to sustain growth performance in gilthead seabream (Sparus aurata) during the grow-out phase. Aquaculture 293, 255–262. CrossRefGoogle Scholar
Dosdat, A., Person-Le Ruyet, J., Covès, D., Dutto, G., Gasset, E., Le Roux, A., Lemarié, G., 2003, Effect of chronic exposure to ammonia on growth, food utilisation and metabolism of the European sea bass (Dicentrarchus labrax). Aquat. Living Resour. 16, 509–520. CrossRefGoogle Scholar
Dudchenko, P.A., 2001, How do animals actually solve the maze? Behav. Neurosci. 115, 850–860. Google Scholar
Figueiredo-Silva, A., Rocha, E., Dias, J., Silva, P., Rema, P., Gomes, E., Valente, L.M.P., 2005, Partial replacement of fish oil by soybean oil on lipid distribution and liver histology in European seabass (Dicentrarchus labrax) and rainbow trout (Oncorhynchus mykiss) juveniles. Aquac. Nutr. 11, 147–155. CrossRefGoogle Scholar
Gaikwad, S., Stewart, A., Hart, P., Wong, K., Piet, V., Cachat, J., Kalueff, A.V., 2011, Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: The utility of fish models to study stress–memory interplay. Behav. Process. 87, 224–230. CrossRefGoogle ScholarPubMed
Ganga, R., Montero, D., Bell, J.G., Atalah, E., Ganuza, E., Vega-Orellana, O., Tort, L., Acerete, L., Afonso, J.M., Benitez-Sanatana, T., Vaquero, A.F., Izquierdo, M., 2011, Stress response in sea bream (Sparus aurata) held under crowded conditions and fed diets containing linseed and/or soybean oil. Aquaculture 311, 215–223. CrossRefGoogle Scholar
Ganga, R., Tort, L., Acerete, L., Montero, D., Izquierdo, M.S., 2006, Modulation of ACTH-induced cortisol release by polyunsaturated fatty acids in interrenal cells from gilthead seabream, Sparus aurata. J. Endocrinol. 190, 39–45. CrossRefGoogle ScholarPubMed
Gibson, B.M., Shettleworth, S.J., 2005, Place versus response learning revisited: tests of blocking on the radial maze. Behav. Neurosci. 119, 567–586. CrossRefGoogle ScholarPubMed
Greene, D.H., Selivonchick, D.P., 1990, Effects of dietary vegetable, animal and marine lipids on muscle lipid and hematology of rainbow trout (Oncorhynchus mykiss). Aquaculture 89, 165–182. CrossRefGoogle Scholar
Guillaume J., Kaushik S., Bergot P., Métailler R., 2001, Nutrition and feeding of fish and crustaceans. Springer-Praxis Publishing, Chichester.
Guillou, A., Soucy, P., Khalil, M., Adambounou, L., 1995, Effects of dietary vegetable and marine lipids on growth, muscle fatty acid composition and organoleptic quality of flesh of brook charr (Salvelinus fontinalis). Aquaculture 136, 351–362. CrossRefGoogle Scholar
Hardy, R.W., Scott, T.M., Harrell, L.W., 1987, Replacement of herring oil with menhaden oil, soybean oil, or tallow in the diets of Atlantic salmon raised in marine net-pens. Aquaculture 65, 267–277. CrossRefGoogle Scholar
Harrenstien, L.A., Tornquist, S.J., Miller-Morgan, T.J., Fodness, B.G., Clifford, K.E., 2005, Evaluation of a point-of-care blood analyzer and determination of reference ranges for blood parameters in rockfish. J. Am. Vet. Med. Assoc. 226, 255–265. CrossRefGoogle ScholarPubMed
Hölscher, C., 1999, Stress impairs performance in spatial water maze tasks. Behav. Brain Res. 100, 225–235. CrossRefGoogle Scholar
Ishizaki, Y., Masuda, R., Uematsu, K., Shimizu, K., Arimoto, M., Takeuchi, T., 2001, The effect of dietary docosahexaenoic acid on schooling behaviour and brain development in larval yellowtail. J. Fish Biol. 58, 1691–1703. CrossRefGoogle Scholar
Izquierdo, M.S., Obach, A., Arantzamendi, L., Montero, D., Robaina, L., Rosenlund, G., 2003, Dietary lipid sources for seabream and seabass: growth performance, tissue composition and flesh quality. Aquac. Nutr. 9, 397–407. CrossRefGoogle Scholar
Kaushik, S., Coves, D., Dutto, G., Blanc, D., 2004, Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the European seabass, Dicentrarchus labrax. Aquaculture 230, 391–404. CrossRefGoogle Scholar
Kohbara, J., Hidaka, I., Matsuoka, F., Osada, T., Furukawa, K., Yamashita, M., Tabata, M., 2003, Self-feeding behavior of yellowtail, Seriola quinqueradiata, in net cages: diel and seasonal patterns and influences of environmental factors. Aquaculture 220, 581–594. CrossRefGoogle Scholar
Laporte, J., Trushenski, J., 2012, Production performance, stress tolerance and intestinal integrity of sunshine bass fed increasing levels of soybean meal. J. Anim. Physiol. Anim. Nutr. 96, 513–526. CrossRefGoogle ScholarPubMed
LeBoucher, R., Vandeputte, M., Dupont-Nivet, M., Quillet, E., Mazurais, D., Robin, J., Vergnet, A., Médale, F., Kaushik, S., Chatain, B., 2011, A first insight into genotype-diet interactions in European sea bass (Dicentrarchus labrax L. 1756) in the context of plant-based diet use. Aquac. Res. 42, 583–592. CrossRefGoogle Scholar
Lim, S.Y., Hoshiba, J., Moriguchi, T., Salem, J.N., 2005, N-3 fatty acid deficiency induced by a modified artificial rearing method leads to poorer performance in spatial learning tasks. Pediatr. Res. 584, 741–748. CrossRefGoogle Scholar
Lopez, J.C., Broglio, C., Rodriguez, F., Thimus-Blanc, C., Salas, C., 1999, Multiple spatial learning strategies in goldfish (Carassius auratus). Anim. Cogn. 2, 109–120. Google Scholar
Malavasi, S., Georgalas, V., Lugli, M., Torricelli, P., Mainardi, D., 2004, Differences in the pattern of antipredator behaviour between hatchery-reared and wild European sea bass juveniles. J. Fish Biol. 65 (Suppl. A), 143–155. CrossRefGoogle Scholar
Marino, G., Di Marco, P., Mandich, A., Finoia, M.G., Cataudella, S., 2001, Changes in serum cortisol, metabolites, osmotic pressure and electrolytes in response to different blood sampling procedures in cultured sea bass (Dicentrarchus labrax L.). J. Appl. Ichthyol. 17, 115–120. CrossRefGoogle Scholar
Martínez-Llorens, S., Vidal, A.T., Moñino, A.V., Torres, M.P., Cerdá, M.J., 2007, Effects of dietary soybean oil concentration on growth, nutrient utilization and muscle fatty acid composition of gilthead bream (Sparus aurata L.). Aquac. Res. 38, 76–81. CrossRefGoogle Scholar
Millot, S., Bégout, M.-L., Chatain, B., 2009, Exploration behaviour and flight response toward a stimulus in three sea bass strains (Dicentrarchus labrax L.). Appl. Anim. Behav. 119, 108–114. CrossRefGoogle Scholar
Millot, S., Bégout, M.-L., Person-Le Ruyet, J., Breuil, G., Di-Poï, C., Fievet, J., Pineau, P., Roué, M., Sévère, A., 2008, Feed demand behavior in sea bass juveniles: effects on individual specific growth rate variation and health (inter-individual and intergroup variation). Aquaculture 274, 87–95. CrossRefGoogle Scholar
Montero, D., Kalinowski, T., Obach, A., Robaina, L., Tort, L., Caballero, M.J., Izquierdo, M.S., 2003, Vegetable lipid sources for gilthead seabream (Sparus aurata): effects on fish health. Aquaculture 225, 353–370. CrossRefGoogle Scholar
Montero, D., Robaina, L., Caballero, M.J., Ginès, R., Izquierdo, M.S., 2005, Growth, feed utilization and flesh quality of European sea bass (Dicentrarchus labrax) fed diets containing vegetable oils: a time-course study on the effect of a refeeding period with a 100% fish oil diet. Aquaculture 248, 121–134. CrossRefGoogle Scholar
Montero D. , Izquierdo M., 2010, Welfare and health of fish fed vegetable oils as alternative lipid sources to fish oil. In: Turchini G.M., Ng W.K., Tocher R.D. (Eds.). Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Taylor & Francis, Boca Raton, FL.
Moriguchi, T., Greiner, R.S., Salem, J.N., 2000, Behavioral deficits associated with dietary induction of decreased brain docohexaenoic acid concentration. J. Neurochem. 756, 2563–2573. Google Scholar
Mourente, G., Dick, J.R., Bell, J.G., Tocher, D.R., 2005, Effect of partial substitution of dietary fish oil by vegetable oils on desaturation and [beta]-oxidation of [1-14C]18:3n-3 and (LNA) and [1-14C]20:5n-3 (EPA) in hepatocytes and enterocytes of European sea bass (Dicentrarchus labrax L.). Aquaculture 248, 173–186. CrossRefGoogle Scholar
Nilsson, J., Kristiansen, T.S., Fosseidengen, J.E., Fernö, A., van den Bos, R., 2008, Sign- and goal-tracking in Atlantic cod (Gadus morhua). Anim. Cogn. 11, 651–659. CrossRefGoogle Scholar
Owada, Y., Abdelwahab, S.A., Kitanaka, N., Sakagami, H., Takano, H., Sugitani, Y., Sugawara, M., Kawashima, H., Kiso, Y., Mobarakeh, J.I., Yanai, K., Kaneko, K., Sasaki, H., Kato, H., Saino-Saito, S., Matsumoto, N., Akaike, N., Noda, T., Kondo, H., 2006, Altered emotional behavioral responses in mice lacking brain-type fatty acid-binding protein gene. Eur. J. Neurosci. 24, 175–187. CrossRefGoogle ScholarPubMed
Peruzzi, S., Varsamos, S., Chatain, B., Fauvel, C., Menu, B., Falguière, J.C., Sévère, A., Flik, G., 2005, Haematological and physiological characteristics of diploid and triploid sea bass, Dicentrarchus labrax L. Aquaculture 244, 359–367. CrossRefGoogle Scholar
Reinitz, G.L., Yu, T.C., 1981, Effects of dietary lipids on growth and fatty acid composition of rainbow trout (salmo gairdneri). Aquaculture 22, 359–366. CrossRefGoogle Scholar
Restle, F., 1957, Discrimination of cues in mazes: A resolution of the “place-vs-response” question. Psychol. Rev. 64, 217–228. CrossRefGoogle Scholar
Roche, H., Boge, G., 1996, Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Mar. Environ. Res. 41, 27–43. CrossRefGoogle Scholar
Rubio, V.C., Vivas, M., Sanchez-Mut, A., Sanchez-Vazquez, F.J., Coves, D., Dutto, G., Madrid, J.A., 2004, Self-feeding of European sea bass (Dicentrarchus labrax L.) under laboratory and farming conditions using a string sensor. Aquaculture 233, 393–403. CrossRefGoogle Scholar
Saillant, E., Fostier, A., Haffray, P., Menu, B., Laureau, S., Thimonier, J., Chatain, B., 2003, Effects of rearing density, size grading and parental factors on sex ratios of the sea bass (Dicentrarchus labrax L.) in intensive aquaculture. Aquaculture 221, 183–206. CrossRefGoogle Scholar
Sánchez-Vázquez, F.J., Martinez, M., Zamora, S., Madrid, J.A., 1994, Design and performance of an accurate demand feeder for the study of feeding behaviour in sea bass, Dicentrarchus labrax L. Physiol. Behav. 56, 789–794. CrossRefGoogle ScholarPubMed
Sargent J., Tocher D.R., Bell J.G., 2002, The lipids. In: Halver J.E., Hardy R.W. (Eds.), Fish Nutrition, Academic Press, San Diego, CA, pp. 59–66.
Schreck, C.B., 1982, Stress and rearing of salmonids. Aquaculture 28, 241–249. CrossRefGoogle Scholar
Serot, T., Regost, C., Arzel, J., 2002, Identification of odour active compounds in muscle of brown trout (Salmo trutta) as affected by dietary lipid sources. J. Sci. Food Agric. 82, 636–643. CrossRefGoogle Scholar
Serot, T., Regost, C., Prost, C., Robin, J., Arzel, J., 2001, Effect of dietary lipid sources on odour-active compounds in muscle of turbot (Psetta maxima). J. Sci. Food Agric. 81, 1339–1346. CrossRefGoogle Scholar
Shapiro, D.Y., 1980, Serial female changes after simultaneous removal of males from social groups of a coral reef fish. Science 209, 1136–1137. CrossRefGoogle Scholar
Siebeck, U.E., Litherland, L., Wallis, G.M., 2009, Shape learning and discrimination in reef fish. J. Exp. Biol. 212, 2113–2119. CrossRefGoogle Scholar
Tacon, A., 1998, FAO aquaculture production update. Int. Aquafeeds 2, 13-16. Google Scholar
Thomassen, M.S., Rosjo, C., 1989, Different fats in feed for salmon: influence on sensory parameters, growth rate and fatty acids in muscle and heart. Aquaculture 79, 129–135. CrossRefGoogle Scholar
Trushenski, J., Schwarz, M., Pessoa, W.V.N., Mulligan, B., Crouse, C., Gause, B., Yamamoto, F., Delbos, B., 2013, Amending reduced fish-meal feeds with marine lecithin, but not soy lecithin, improves the growth of juvenile cobia and may attenuate heightened responses to stress challenge. J. Anim. Physiol. Anim. Nutr. 97, 170–180. CrossRefGoogle Scholar
Van Anholt, R.D., Koven, W.M., Lutzky, S., WendelaarBonga, S.E., 2004, Dietary supplementation with arachidonic acid alters the stress response of gilthead seabream (Sparus aurata) larvae. Aquaculture 238, 369–383. CrossRefGoogle Scholar
Watanabe, T., Verakunpiriya, V., Watanabe, K., Viswanath, K., Satoh, S., 1998, Feeding of rainbow trout with non-fish meal diets. Fish Sci. 63, 258–266. CrossRefGoogle Scholar