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Seasonal and diurnal variability in carbon respiration, calcification and excretion rates of the abalone Haliotis tuberculata L.

Published online by Cambridge University Press:  12 March 2018

Coraline Chapperon ,
Jacques Clavier ,
Clément Dugué ,
Erwan Amice ,
Manon Le Goff  and
Sabine Roussel
Coraline Chapperon
Affiliation:
Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France School of Biological Sciences, Flinders University, Sturt Rd, Bedford Park, Adelaide, 5042, South Australia
Jacques Clavier
Affiliation:
Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France
Clément Dugué
Affiliation:
Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France
Erwan Amice
Affiliation:
Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France
Manon Le Goff
Affiliation:
Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France
Sabine Roussel*
Affiliation:
Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France
*
Correspondence should be addressed to: S. Roussel, Laboratoire des Sciences de l'Environnement Marin (LEMAR), UMR 6539 UBO, CNRS, IRD, IFREMER, Institut Universitaire Européen de la Mer (IUEM), rue Dumont d'Urville, 29280 Plouzané, France email: [email protected]
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Abstract

Abalone (Haliotis spp.) are commercially important marine shellfish species worldwide. Knowledge about the physiology of abalone that impacts life-history traits is important for a better understanding of the biology of the species and the impact of stressful husbandry procedures at different seasons. The present study quantified the seasonal and diurnal variations in four physiological parameters of the European species Haliotis tuberculata, i.e. carbon aerial and aquatic respiration, calcification and excretion rates, and the effect of prolonged aerial exposure upon abalone aerial respiration. We also investigated the effect of individual size upon these physiological parameters. Aquatic respiration and calcification rates showed an allometric relationship with biomass. All parameters showed lower rates in cool season and higher rates in warmer season. Temperature was assumed to be the primary driver of the reported seasonal variability in physiological parameters, although reproductive needs and nutrition may also contribute to the observed patterns. Importantly, abalone did not stop calcifying in winter, and calcified more at night than during the day. Abalone did not respire more underwater at night-time than at daytime, however they excreted more overnight. The low air:aquatic ratio (0.2) is likely to be an energy-saving strategy for emerged H. tuberculata individuals. This study highlights the temporal heterogeneity in physiological rates of H. tuberculata, which constitutes a species recently domesticated in Europe.

Keywords

ormermetabolismcarbon fluxesphysiology
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 2 , March 2019 , pp. 393 - 402
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

REFERENCES

Ahmed, F., Segawa, S., Yokota, M. and Watanabe, S. (2008) Effect of light on oxygen consumption and ammonia excretion in Haliotis discus discus, H. gigantea, H. madaka and their hybrids. Aquaculture 279, 160–165.Google Scholar
Allen, V.J., Marsden, I.D., Ragg, N.L.C. and Gieseg, S. (2006) The effects of tactile stimulants on feeding, growth, behaviour, and meat quality of cultured Blackfoot abalone, Haliotis iris. Aquaculture 257, 294–308.Google Scholar
Baldwin, J., Wells, R.M.G., Low, M. and Ryder, J.M. (1992) Tauropine and D-lactate as metabolic stress indicators during transport and storage of live paua, (New Zealand abalone) (Haliotis iris). Journal of Food Science 57, 280–282.Google Scholar
Barkai, R. and Griffiths, C.L. (1987) Consumption, absorption efficiency, respiration and excretion in the South African abalone Haliotis midae. South African Journal of Marine Science 5, 523–529.Google Scholar
Basuyaux, O., Mathieu, M. and Richard, O. (2001) Influence de Ia taille, de la température et du régime alimentaire sur la consommation d'oxygène de l'oursin. Marine Life 11, 57–67.Google Scholar
Bayne, B.L. and Newell, R.C. (1983) Physiological energetics of marine molluscs. The Mollusca 4, 407–515.Google Scholar
Bayne, B.L. and Scullard, C. (1977) Rates of nitrogen excretion by species of Mytilus (Bivalvia, Mollusca). Journal of the Marine Biological Association of the United Kingdom 57, 355–369.Google Scholar
Buen-Ursua, S.M.A. and Ludevese, G. (2011) Temperature and size range for the transport of juvenile donkey's ear abalone Haliotis asinina Linne. Aquaculture Research 42, 1206–1213.Google Scholar
Carefoot, T.H., Taylor, B.E. and Donovan, D.A. (1998) Seasonality in digestive-gland size and metabolism in relation to reproduction in Haliotis kamtschatkana. Journal of Shellfish Research 17, 713–716.Google Scholar
Chiou, T.K., Lai, M.M. and Shiau, C.Y. (2001) Seasonal variations of chemical constituents in the muscle and viscera of small abalone fed different diets. Fisheries Science 67, 146–156.Google Scholar
Clavier, J., Castets, M.-D., Bastian, T., Hily, C., Boucher, G. and Chauvaud, L. (2009) An amphibious mode of life in the intertidal zone: aerial and underwater contribution of Chthamalus montagui to CO2 fluxes. Marine Ecology Progress Series 375, 185–194.Google Scholar
Clavier, J. and Chardy, P. (1989) Investigation into the ecology of the ormer (Haliotis tuberculata L.), factors influencing spatial distribution. Aquatic Living Resources 2, 191–197.Google Scholar
Clavier, J. and Richard, O. (1982) Etude expérimentale du déplacement de l'ormeau (Haliotis tuberculata) dans le milieu naturel. Revue des Travaux de l'Institut des Pêches Maritimes 46, 315–326.Google Scholar
Clavier, J. and Richard, O. (1986) Growth of juvenile Haliotis tuberculata (Mollusca: Gastropoda) in their natural environment. Journal of the Marine Biological Association of the United Kingdom 66, 497–503.Google Scholar
Cook, P.A. (2014) The worldwide abalone industry. Modern Economy 5, 1181–1186.Google Scholar
Cooke, S.J., Blumstein, D.T., Buchholz, R., Caro, T., Fernández-Juricic, E., Franklin, C.E., Metcalfe, J., O'Connor, C.M., Clair, C.C.S., Sutherland, W.J. and Wikelski, M. (2014) Physiology, behavior, and conservation. Physiological and Biochemical Zoology 87, 1–14.Google Scholar
Crofts, D.R. (1929) Haliotis. Proceedings of the Liverpool Biological Society 43, 1–174 (LMBC Mem. No. 29).Google Scholar
Cunningham, S.C., Smith, A.M. and Lamare, M.D. (2016) The effects of elevated pCO2 on growth, shell production and metabolism of cultured juvenile abalone, Haliotis iris. Aquaculture Research 47, 2375–2392.Google Scholar
Day, R. W. and Quinn, G. P. (1989) Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59, 433–463.Google Scholar
Dickson, A.G. and Goyet, C. (1994) Handbook of methods for the analysis of the various parameters of the carbon dioxide system in sea water. Version 2. Oak Ridge, TN: Oak Ridge National Laboratory.Google Scholar
Dion, P. and Le Bozec, S. (1996) The French Atlantic coasts. In Schramm, W. and Nienhuis, P.H. (eds) Marine benthic vegetation. Berlin: Springer, pp. 251–264.Google Scholar
Forster, G.R. (1967) The growth of Haliotis tuberculata: results of tagging experiments in Guernsey 1963–65. Journal of the Marine Biological Association of the United Kingdom 47, 287–300.Google Scholar
Frankignoulle, M., Canon, C. and Gattuso, J.P. (1994) Marine calcification as a source of carbon dioxide: positive feedback of increasing atmospheric CO2. Limnology and Oceanography 39, 458–462.Google Scholar
Gao, X., Xian, L., Meijie, L., Changbin, S. and Ying, L. (2016) Effects of light intensity on metabolism and antioxidant defense in Haliotis discus hannai Ino. Aquaculture 465, 78–87.Google Scholar
Gaty, G. and Wilson, J.H. (1986) Effect of body size, starvation, temperature and oxygen tension on the oxygen consumption of hatchery-reared ormers Haliotis tuberculata L. Aquaculture 56, 229–237.Google Scholar
Gazeau, F., Alliouane, S., Bock, C., Bramanti, L., López Correa, M., Gentile, M., Hirse, T., Pörtner, H.-O. and Ziveri, P. (2014) Impact of ocean acidification and warming on the Mediterranean mussel (Mytilus galloprovincialis). Frontiers in Marine Science 1, 1–12.Google Scholar
Gazeau, F., Urbini, L., Cox, T.E., Alliouane, S. and Gattuso, J.P. (2015) Comparison of the alkalinity and calcium anomaly techniques to estimate rates of net calcification. Marine Ecology Progress Series 527, 1–12.Google Scholar
González, R.C., Brokordt, K. and Lohrmann, K. B. (2012) Physiological performance of juvenile Haliotis rufescens and Haliotis discus hannai abalone exposed to the withering syndrome agent. Journal of Invertebrate Pathology 111, 20–26.Google Scholar
Hatae, K., Nakai, H., Shimada, A., Murakami, T., Takada, K., Shirojo, Y. and Watabe, S. (1995) Abalone (Hariltis discus): seasonal variations in chemical composition and textural properties. Journal of Food Science 60, 32–35.Google Scholar
Hayashi, I. (1980a) The reproductive biology of the ormer, Haliotis tuberculata. Journal of the Marine Biological Association of the United Kingdom 60, 415–430.Google Scholar
Hayashi, I. (1980b) Structure and growth of a shore population of the ormer, Haliotis tuberculata. Journal of the Marine Biological Association of the United Kingdom 60, 431–437.Google Scholar
Hayashi, I. (1983) Seasonal changes in condition factors and in the C:N ratio of the foot of the ormer, Haliotis tuberculata. Journal of the Marine Biological Association of the United Kingdom 63, 85–95.Google Scholar
Jolivet, A., Chauvaud, L., Huchette, S., Legoff, C., Thébault, J., Nasreddine, K., Schöne, B.R. and Clavier, J. (2015) The ormer (Haliotis tuberculata): a new, promising paleoclimatic tool. Palaeogeography, Palaeoclimatology, Palaeoecology 427, 32–40.Google Scholar
Kenny, R. (1977) Growth studies of the tropical intertidal limpet Acmaea antillarum. Marine Biology 39, 161–170.Google Scholar
Koroleff, F. (1969) Direct determination of ammonia in natural waters as indophenol blue. International Council for the Exploration of the Sea 9, 1–6.Google Scholar
Lachambre, S., Huchette, S., Day, R., Boudry, P., Rio-Cabello, A., Fustec, T. and Roussel, S. (2017) Relationships between growth, survival, physiology and behaviour – a multi-criteria approach to Haliotis tuberculata phenotypic traits. Aquaculture 467, 190–197.Google Scholar
Lejart, M., Clavier, J., Chauvaud, L. and Hily, C. (2012) Respiration and calcification of Crassostrea gigas: contribution of an intertidal invasive species to coastal ecosystem CO2 fluxes. Estuaries and Coasts 35, 622–632.Google Scholar
Lorrain, A., Clavier, J., Thébault, J., Tremblay-Boyer, L., Houlbrèque, F., Amice, E., Le Goff, M. and Chauvaud, L. (2015) Variability in diel and seasonal in situ metabolism of the tropical gastropod Tectus niloticus. Aquatic Biology 23, 167–182.Google Scholar
Lu, J., Shi, Y., Cai, S. and Feng, J. (2017) Metabolic responses of Haliotis diversicolor to Vibrio parahaemolyticus infection. Fish and Shellfish Immunology 60, 265–274.Google Scholar
Marsden, I.D., Shumway, S.E. and Padilla, D.K. (2012) Does size matter? The effects of body size and declining oxygen tension on oxygen uptake in gastropods. Journal of the Marine Biological Association of the United Kingdom 92, 1603–1617.Google Scholar
Martin, S., Thouzeau, G., Chauvaud, L., Jean, F., Guérin, L.and Clavier, J. (2006) Respiration, calcification, and excretion of the invasive slipper limpet, Crepidula fornicata L.: implications for carbon, carbonate, and nitrogen fluxes in affected areas. Limnology and Oceanography 51, 1996–2007.Google Scholar
Martin, S., Thouzeau, G., Richard, M., Chauvaud, L., Jean, F. and Clavier, J. (2007) Benthic community respiration in areas impacted by the invasive mollusk Crepidula fornicata. Marine Ecology Progress Series 347, 51–60.Google Scholar
Mateos, H.T., Lewandowski, P.A. and Su, X.Q. (2010) Seasonal variations of total lipid and fatty acid contents in muscle, gonad and digestive glands of farmed Jade Tiger hybrid abalone in Australia. Food Chemistry 123, 436–441.Google Scholar
Momma, H. and Sato, R. (1970) The locomotion behavior of the disc abalone, Haliotis discus hannai Ino, in a tank. Tohoku Journal of Agricultural Research 21, 20–25.Google Scholar
Morash, A.J. and Alter, K. (2016) Effects of environmental and farm stress on abalone physiology: perspectives for abalone aquaculture in the face of global climate change. Reviews in Aquaculture 8, 342–368.Google Scholar
Newell, R.C. (1973) Factors affecting the respiration of intertidal invertebrates. Integrative and Comparative Biology 13, 513–528.Google Scholar
Pierrot, D., Lewis, E. and Wallace, D.W.R. (2006) MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Oak Ridge, TN: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy.Google Scholar
Pohlert, T. (2014) The pairwise multiple comparison of mean ranks package (PMCMR). R package. http://CRAN.R-project.org/package=PMCMR.Google Scholar
Ragg, N.L.C. and Watts, E. (2015) Physiological indicators of stress and morbidity in commercially handled abalone Haliotis iris. Journal of Shellfish Research 34, 455–467.Google Scholar
Roussel, S., Huchette, S., Clavier, J. and Chauvaud, L. (2011) Growth of the European abalone (Haliotis tuberculata L.) in situ: seasonality and ageing using stable oxygen isotopes. Journal of Sea Research 65, 213–218.Google Scholar
Roussel, V., Charreyron, J., Labarre, S., Van Wormhoudt, A. and Huchette, S. (2013) First steps on technological and genetic improvement of European abalone (Haliotis tuberculata) based on investigations in full-sib families. Open Journal of Genetics 3, 224–233.Google Scholar
Roy, R.N., Roy, L.N., Vogel, K.M., Porter-Moore, C., Pearson, T., Good, C.E., Millero, F.J. and Campbell, D.M. (1993) The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. Marine Chemistry 44, 249–267.Google Scholar
Sakai, S. (1960) On the formation of the annual ring on the shell of the abalone Haliotis discus var Hannai ino. Tohoku Journal of Agricultural Research 11, 239–244.Google Scholar
Shepherd, S.A. (1973) Studies on southern Australian abalone (genus Haliotis). I. Ecology of five sympatric species. Australian Journal of Marine and Freshwater Research 24, 217–258.Google Scholar
Smith, S.V. and Key, G.S. (1975) Carbon dioxide and metabolism in marine environments. Limnology and Oceanography 20, 493–495.Google Scholar
Somero, G.N. (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integrative and Comparative Biology 42, 780–789.Google Scholar
Sororzano, L. (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnology Oceanography 14, 799–801.Google Scholar
Stephenson, T.A. (1924) Notes on Haliotis tuberculata. I. Journal of the Marine Biological Association of the United Kingdom 13, 480–495.Google Scholar
Su, X.Q., Antonas, K., Li, D. and Nichols, P. (2006) Seasonal variations of total lipid and fatty acid contents in the muscle of two Australian farmed abalone species. Journal of Food Lipids 13, 411–423.Google Scholar
Tagliarolo, M., Clavier, J., Chauvaud, L. and Grall, J. (2013a) Carbon emission associated with respiration and calcification of nine gastropod species from the intertidal rocky shore of Western Europe. Marine Biology 160, 2891–2901.Google Scholar
Tagliarolo, M., Clavier, J., Chauvaud, L., Koken, M. and Grall, J. (2012) Metabolism in blue mussel: intertidal and subtidal beds compared. Aquatic Biology 17, 167–180.Google Scholar
Tagliarolo, M., Grall, J., Chauvaud, L. and Clavier, J. (2013b) Aerial and underwater metabolism of Patella vulgata L.: comparison of three intertidal levels. Hydrobiologia 702, 241–253.Google Scholar
Taylor, H.H. and Ragg, N.L.C. (2005) The role of body surfaces and ventilation in gas exchange of the abalone, Haliotis iris. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 175, 463–478.Google Scholar
Travers, M.A., Le Goic, N., Huchette, S., Koken, M. and Paillard, C. (2008) Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection. Fish & Shellfish Immunology 25, 800–808.Google Scholar
Uki, N. and Kikuchi, S. (1975) Oxygen consumption of the abalone, Haliotis discus hannai in relation to body size and temperature. Bulletin of Tohoku Regional Fisheries Research Laboratory 35, 73–84.Google Scholar
van Wormhoudt, A., Gaume, B., Le Bras, Y., Roussel, V. and Huchette, S. (2011) Two different and functional nuclear rDNA genes in the abalone Haliotis tuberculata: tissue differential expression. Genetica 139, 1217–1227.Google Scholar
Vaughn, C.C. and Hakenkamp, C.C. (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46, 1431–1446.Google Scholar
Wells, R.M.G. and Baldwin, J. (1995) A comparison of metabolic stress during air exposure in two species of New Zealand abalone, Haliotis iris and Haliotis australis: implications for the handling and shipping of live animals. Aquaculture 134, 3–4.Google Scholar
Werner, I., Flothmann, S. and Burnell, G. (1995) Behaviour studies on the mobility of two species of abalone (Haliotis tuberculata and H. discus hannai) on sand: implications for reseeding programmes. Marine and Freshwater Research 46, 681–688.Google Scholar
Widdows, J. and Shick, J.M. (1985) Physiological responses of Mytilus edulis and Cardium edule to aerial exposure. Marine Biology 85, 217–232.Google Scholar
Young, J.L., Bornik, Z.B., Marcotte, M.L., Charlie, K.N., Wagner, G.N., Hinch, S.G. and Cooke, S.J. (2006) Integrating physiology and life history to improve fisheries management and conservation. Fish and Fisheries 7, 262–283.Google Scholar