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Allometric size-scaling of biometric growth parameters and metabolic and excretion rates. A comparative study of intertidal and subtidal populations of mussels (Mytilus galloprovincialis)

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Abstract

Allometric relationships between biometric parameters (i.e., soft body and shell weights and shell organic content vs. shell length) as well as for routine and standard metabolic and ammonia excretion rates related to flesh weight and shell length were estimated and compared for subtidal and intertidal populations of Mytilus galloprovincialis in Galicia (NW Spain). This is the first report on allometric size-scaling of excretion and metabolic (both routine and standard) rates in this species. No evidences of differences in size exponent were found between physiological rates or between both populations for any physiological rate. Intercepts of regression lines were significantly higher in subtidal than in intertidal mussels, indicating greater levels of energy expenditure in the former. However, metabolic scope for feeding and growth was about two-fold in intertidal mussels, pointing to a reduced growth efficiency compared with subtidal mussels. Evolution of biometric parameters of body components with size indicated that subtidal mussels allocated energy resources preferably into flesh growth, achieving higher condition indices, while intertidal mussels put more effort on shell calcification and thickening which resulted in heavier shells of reduced organic content. These differentiated growth “strategies” of both populations could be related to their differences in growth efficiencies.

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References

  • Akester, R. J. & A. L. Martel, 2000. Shell shape, dysodont tooth morphology, and hinge-ligament thickness in the bay mussel Mytilus trossulus correlate with wave exposure. Canadian Journal of Zoology 78: 240–253.

    Article  Google Scholar 

  • Aldrich, J. C. & M. Crowley, 1986. Condition and variability in Mytilus edulis (L.) from different habitats in Ireland. Aquaculture 52: 273–286.

    Article  Google Scholar 

  • Anestis, A., H. O. Pörtner, D. Karagiannis, P. Angelidis, A. Staikou & B. Michaelidis, 2010. Response of Mytilus galloprovincialis (L.) to increasing seawater temperature and to marteliosis: metabolic and physiological parameters. Comparative Biochemistry and Physiology, Part A 156: 57–66.

    Article  Google Scholar 

  • Atanasov, A. T. & D. B. Dimitrov, 2002. Changes of the power coefficient in the ‘metabolism-mass’ relationship in the evolutionary process of animals. BioSystems 66: 65–71.

    Article  PubMed  Google Scholar 

  • Babarro, J. M. F., M. J. Fernández-Reiriz & U. Labarta, 2000a. Feeding behaviour of seed mussel Mytilus galloprovincialis: environmental parameters and seed origin. Journal of Shellfish Research 19: 195–201.

    Google Scholar 

  • Babarro, J. M. F., M. J. Fernández-Reiriz & U. Labarta, 2000b. Metabolism of the mussel Mytilus galloprovincialis from two origins in the Ría de Arousa (north-west Spain). Journal of the Marine Biological Association of the United Kingdom 80: 865–872.

    Article  Google Scholar 

  • Babarro, J. M. F., U. Labarta & M. J. Fernández-Reiriz, 2003. Growth patterns in biomass and size structure of Mytilus galloprovincialis cultivated in the “Ría de Arousa” (north-west Spain). Journal of the Marine Biological Association of the United Kingdom 83: 151–158.

    Article  Google Scholar 

  • Bayne, B. L. & R. C. Newell, 1983. Physiological energetics of marine molluscs. In Saleuddin, A. S. M. & K. M. Wilbur (eds), The Mollusca, Vol. 4. Physiology, Part 1. Academic Press, New York: 407–515.

    Google Scholar 

  • Bayne, B. L. & C. J. Scullard, 1977. Rates of nitrogen excretion by species of Mytilus (Bivalvia: Mollusca). Journal of the Marine Biological Association of the United Kingdom 57: 355–369.

    Article  CAS  Google Scholar 

  • Bayne, B. L., R. J. Thompson & J. Widdows, 1973. Some effects of temperature and food on the rate of oxygen consumption by Mytilus edulis L. In Weiser, W. (ed.), Effects of Temperature on Ectothermic Organisms. Springer, Berlin: 181–193.

    Chapter  Google Scholar 

  • Bayne, B. L., C. J. Bayne, T. C. Carefoot & R. J. Thompson, 1976a. The physiological ecology of Mytilus californianus Conrad. Oecologia 22: 229–250.

    Article  Google Scholar 

  • Bayne, B. L., J. Widdows & A. Thompson, 1976b. Physiological integrations. In Bayne, B. L. (ed), Marine Mussels: Their Ecology and Physiology, 1st ed Cambridge University Press, Cambridge: 261–291.

    Google Scholar 

  • Bayne, B. L., A. J. S. Hawkins & E. Navarro, 1988. Feeding and digestion in suspension-feeding bivalve mollusks – the relevance of physiological compensations. American Zoologist 28: 147–159.

    Article  Google Scholar 

  • Bayne, B. L., A. J. S. Hawkins, E. Navarro & J. I. P. Iglesias, 1989. Effects of seston concentration on feeding, digestion and growth in the mussel Mytilus edulis. Marine Ecology Progress Series 55: 47–54.

    Article  Google Scholar 

  • Bokma, F., 2004. Evidence against universal metabolic allometry. Functional Ecology 18: 184–187.

    Article  Google Scholar 

  • Borrero, F. J. & T. J. Hilbish, 1988. Temporal variation in shell and soft tissue growth of the mussel Geukensia demissa. Marine Ecology Progress Series 42: 9–15.

    Article  Google Scholar 

  • Brookes, J. I., 2006. Proximate control and microstructure characteristics of predator-induced shell thickening in the intertidal gastropod Littorina obtusata. University of New Brunswick, Fredericton.

    Google Scholar 

  • Brookes, J. I. & R. Rochette, 2007. Mechanism of a plastic phenotypic response: predator-induced shell thickening in the intertidal gastropod Littorina obtusata. Journal of Evolutionary Biology 20: 1015–1027.

    Article  CAS  PubMed  Google Scholar 

  • Brown, R. A. & R. Seed, 1977. Modiolus modiolus – an autecological study. In: Keegan, B. F., P. O’Ceidigh & P. J. S. Boaden, (eds) Proceedings on 11th European Marine Biology Symposium, Pergamon Press, Oxford: 93–100

  • Carey, N., J. D. Sigwart & J. G. Richards, 2013. Economies of scaling: more evidence that allometry of metabolism is linked to activity, metabolic rate and habitat. Journal of Experimental Marine Biology and Ecology 439: 7–14.

    Article  Google Scholar 

  • Dame, R. F., 2012. Ecology of Marine Bivalves: An Ecosystem Approach, 2nd ed CRC Press, Boca Raton.

    Google Scholar 

  • Dickie, L. M., P. R. Boudreaup & F. R. Freeman, 1984. Influences of stock and site on growth and mortality in the blue mussel (Mytilus edulis). Canadian Journal of Fisheries and Aquatic Sciences 41: 225–236.

    Article  Google Scholar 

  • Duarte, P., M. J. Fernández-Reiriz, R. A. Filgueira & U. Labarta, 2010. Modelling mussel growth in ecosystems with low suspended matter loads. Journal of Sea Research 64: 273–286.

    Article  Google Scholar 

  • Elvin, O. W. & J. J. Gonor, 1979. The thermal regime of an intertidal Mytilus californianus Conrad population on the central Oregon coast. Journal of Experimental Marine Biology and Ecology 39: 265–279.

    Article  Google Scholar 

  • Fox, D. L. & W. R. Coe, 1943. Biology of the Californian sea mussel (Mytilus californianus). II. Nutrition, metabolism, growth and calcium deposition. Journal of Experimental Zoology 93: 203–249.

    Article  Google Scholar 

  • Freeman, K. R., 1974. Growth, mortality and seasonal cycle of Mytilus edulis in two Nova Scotian embayments. Department of the Environment, Fisheries and Marine Service, Technical Report N° 500: 1–112.

  • Freeman, A. S., 2007. Specificity of induced defenses in Mytilus edulis and asymmetrical predator deterrence. Marine Ecology Progress Series 334: 145–153.

    Article  Google Scholar 

  • Freites, L., M. J. Fernández-Reiriz & U. Labarta, 2002. Lipid classes of mussel seeds Mytilus galloprovincialis of subtidal and rocky shore origin. Aquaculture 207: 97–111.

    Article  CAS  Google Scholar 

  • Gardner, J. P. A. & M. L. H. Thomas, 1987. Growth, mortality and production of organic matter by a rocky intertidal population of Mytilus edulis in the Quoddy Region of the Bay of Fundy. Marine Ecology Progress Series 39: 31–36.

    Article  Google Scholar 

  • Glazier, D. S., 2005. Beyond the “3/4-power law”: variation in the intra- and interspecific scaling of metabolic rate in animals. Biological Reviews of the Cambridge Philosophical Society 80: 611–662.

    Article  PubMed  Google Scholar 

  • Glazier, D. S., 2008. Effects of metabolic level on the body-size scaling of metabolic rate in birds and mammals. Proceedings of the Royal Society of London B 275: 1405–1410.

    Article  Google Scholar 

  • Glazier, D. S., 2009a. Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. Journal of Comparative Physiology B 179: 821–828.

    Article  Google Scholar 

  • Glazier, D. S., 2009b. Metabolic level and size-scaling of rates of respiration and growth in unicellular organisms. Functional Ecology 23: 963–968.

    Article  Google Scholar 

  • Glazier, D. S., 2009c. Ontogenetic body-mass scaling of resting metabolic rate covaries with species-specific metabolic level and body size in spiders and snakes. Comparative Biochemistry and Physiology Part A 153: 403–407.

    Article  Google Scholar 

  • Glazier, D. S., 2010. A unifying explanation for diverse metabolic scaling in animals and plants. Biological Reviews 85: 111–138.

    Article  PubMed  Google Scholar 

  • Gosling, E., 2003. Bivalve molluscs: Biology, Ecology and Culture. Blackwell Science, Oxford: 443.

    Book  Google Scholar 

  • Goulletquer, O. & M. Wollowitz, 1989. The shell of Cardium edule, Cardium glaucum and Ruditapes philippinarum. Organic content, composition and energy value as determined by different methods. Journal of the Marine Biological Association of the United Kingdom 69: 563–572.

    Article  Google Scholar 

  • Griffiths, C. L. & R. J. Griffiths, 1987. Bivalvia. In Pandian, T. J. & F. J. Vernberg (eds), Animal Energetics, Vol. 2, Bivalvia Through Reptilia. Academic Press, Cambridge: 1–87.

    Chapter  Google Scholar 

  • Griffiths, C. L. & J. A. King, 1979. Some relationship between size, food availability and energy balance in the ribbed mussel Aulacomya ater. Marine Biology 51: 141–149.

    Article  Google Scholar 

  • Hawkins, A. J. S. & B. L. Bayne, 1985. Seasonal variation in the relative utilization of carbon and nitrogen by the mussel Mytilus edulis: budgets, conversion efficiencies and maintenance requirements. Marine Ecology Progress Series 25: 181–188.

    Article  CAS  Google Scholar 

  • Hawkins, A. J. S. & B. L. Bayne, 1992. Physiological interrelations, and the regulation of production. In Gosling, E. (ed), The Mussel Mytilus: Ecology, Physiology, Genetics and Culture. Elsevier Science, Amsterdam: 171–222.

    Google Scholar 

  • Hemachandra, D. & S. Thippeswamy, 2008. Allometry and condition index in green mussel Perna viridis (L.) from St Mary’s Island off Malpe, near Udupi, India. Aquaculture Research 39: 1747–1758.

    Article  Google Scholar 

  • Hilbish, T. J., 1986. Growth trajectories of shell and soft tissue in bivalves: seasonal variation in Mytilus edulis L. Journal of Experimental Marine Biology and Ecology 96: 103–113.

    Article  Google Scholar 

  • Jensen, M., Q. P. Fitzgibbon, C. G. Carter & L. R. Adams, 2013. Effect of body mass and activity on the metabolic rate and ammonia-N excretion of the spiny lobster Sagmariasus verreauxi during ontogeny. Comparative Biochemistry and Physiology Part A 166: 191–198.

    Article  CAS  Google Scholar 

  • Jørgensen, C. B., 1976. Growth efficiencies and factors controlling size in some mytilid bivalves, especially Mytilus edulis L.: review and interpretation. Ophelia 15: 175–192.

    Article  Google Scholar 

  • Labarta, U., M. J. Fernandez-Reiriz & J. M. F. Babarro, 1997. Differences in physiological energetics between intertidal and raft cultivated mussels Mytilus galloprovincialis. Marine Ecology Progress Series 152: 167–173.

    Article  Google Scholar 

  • Labarta U., M. J. Fernández-Reiriz, A. Pérez-Camacho& A. P. Corbacho, 2004. Bateeiros, mar, mejillón. Una perspectiva bioeconómica. Centro de Investigaciones Económicas y Financieras (CIEF). Fundación CaixaGalicia. Santiago de Compostela.

  • Leonard, G. H., M. D. Bertness & P. O. Yund, 1999. Crab predation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. Ecology 80: 1–14.

    Article  Google Scholar 

  • Mallet, A. L., C. E. A. Carver, S. S. Coffen & K. R. Freeman, 1987. Winter growth of the blue mussel Mytilus edulis L.: importance of stock and site. Journal of Experimental Marine Biology and Ecology 108: 217–228.

    Article  Google Scholar 

  • Marsden, I. D. & M. A. Weatherhead, 1999. Shore-level induced variations in condition and feeding of the mussel Perna canaliculus from the east coast of the South Island, New Zealand. New Zealand Journal of Marine Freshwater Research 33: 611–622.

    Article  Google Scholar 

  • Muller-Landau, H. C., R. S. Condit, J. Chave, S. C. Thomas, S. A. Bohlman, S. Bunyavejchewin, S. Davies, R. Foster, S. Gunatilleke, K. E. Harms, T. Hart, S. P. Hubbell, A. Itoh, A. R. Kassim, J. V. La Frankie, H. S. Lee, E. Losos, J. R. Makana, T. Ohkubo, R. Sukumar, I. F. Sun, N. Supardi, S. Tan, J. Thompson, R. Valencia, G. V. Muñoz, C. Wills, T. Yamakura, G. Chuyong, H. S. Dattaraja, S. Esufali, P. Hall, C. Hernandez, D. Kenfack, S. Kiratiprayoon, H. S. Suresh, D. Thomas, M. I. Vallejo & P. Ashton, 2006. Testing metabolic ecology theory for allometric scaling of tree size, growth and mortality in tropical forests. Ecology Letters 9: 575–588.

    Article  PubMed  Google Scholar 

  • Naddafi, R. & L. G. Rudstam, 2014. Predator-induced morphological defences in two invasive dreissenid mussels: implications for species replacement. Freshwater Biology 59: 703–713.

    Article  Google Scholar 

  • Navarro, E., J. I. P. Iglesias, A. P. Camacho, U. Labarta & R. Beiras, 1991. The physiological energetics of mussels (Mytilus galloprovincialis Lmk.) from different cultivation rafts in the Ria de Arosa (Galicia N.W. Spain). Aquaculture 94: 197–212.

    Article  Google Scholar 

  • Okumuş, I. & H. P. Stirling, 1994. Physiological energetics of cultivated mussel (Mytilus edulis) populations in 2 Scottish west coast sea lochs. Marine Biology 119: 125–131.

    Article  Google Scholar 

  • Pérez-Camacho, A., U. Labarta & R. Beiras, 1995. Growth of mussels (Mytilus edulis galloprovincialis) on cultivation rafts: influence of seed source, cultivation site and phytoplankton availability. Aquaculture 138: 349–362.

    Article  Google Scholar 

  • Pérez-Camacho, A., U. Labarta, V. Vinseiro & M. J. Fernandez-Reiriz, 2013. Mussel production management: raft culture without thinning-out. Aquaculture 406–407: 172–179.

    Article  Google Scholar 

  • Pérez-Camacho, A., E. Aguiar, U. Labarta, V. Vinseiro, M. J. Fernández-Reiriz & X. A. Álvarez-Salgado, 2014. Ecosystem-based indicators as a tool for mussel culture management strategies. Ecological Indicators 45: 538–548.

    Article  Google Scholar 

  • Peterson, C. H. & R. Black, 1988. Responses of growth to elevation fail to explain vertical zonation of suspension-feeding bivalves on a tidal flat. Oecologia 76: 423–429.

    Article  Google Scholar 

  • Prosser, C. L., 1973. Oxygen: respiration and metabolism. In Prosser, C. L. (ed.), Comparative Animal Physiology, Vol. 1. Saunders College, Philadelphia: 165–211.

    Google Scholar 

  • Rao, K. P., 1953. Shell weight as a function of intertidal height in a littoral population of pelecypods. Experentia 9: 465–466.

    Article  Google Scholar 

  • Raubenheimer, D. & P. Cook, 1990. Effects of exposure to wave action on allocation of resources to shell and meat growth by the subtidal mussel, Mytilus californianus. Journal of Shellfish Research 9: 87–93.

    Google Scholar 

  • Rawson, P. D. & T. J. Hilbish, 1991. Genotype-environment interaction for juvenile growth in the hard clam Mercenaria mercenaria (L.). Evolution 45: 1924–1935.

    Article  Google Scholar 

  • Reich, P. B., M. G. Tjoelker, J. L. Machado & J. Oleksyn, 2006. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439: 457–461.

    Article  CAS  PubMed  Google Scholar 

  • Riisgård, H. U., 1998. No foundation of a ‘3/4 power scaling law’ for respiration in biology. Ecology Letters 1: 71–73.

    Article  Google Scholar 

  • Rodhouse, P. G., C. M. Roden, M. P. Hensey & T. H. Ryan, 1984. Resource allocation in Mytilus edulis on the shore and in suspended culture. Marine Biology 84: 27–34.

    Article  Google Scholar 

  • Sarà, G. & A. Pusceddu, 2008. Scope for growth of Mytilus galloprovincialis (Lmk., 1819) in oligotrophic coastal waters (Southern Tyrrhenian Sea, Italy). Marine Biology 156: 117–126.

    Article  Google Scholar 

  • Seed, R., 1973. Absolute and allometric growth in the mussel, Mytilus edulis L. (Mollusca Bivalvia). Proceedings of the Malacological Society of London 40: 343–357.

    Google Scholar 

  • Shick, J. M., J. Widdows & E. Gnaiger, 1988. Calorimetric studies of behaviour, metabolism and energetics of sessile intertidal animals. American Zoologist 28: 161–181.

    Article  Google Scholar 

  • Smaal, A. C. & M. R. Stralen, 1990. Average annual growth and condition of mussel as a function of food source. Hydrobiologia 195: 179–188.

    Article  Google Scholar 

  • Solórzano, L., 1969. Determination of ammonia in natural waters by the phenolphypoclorite method. Limnology and Oceanography 14: 779–801.

    Article  Google Scholar 

  • Steffani, C. N. & G. M. Branch, 2003. Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Marine Ecology Progress Series 246: 197–209.

    Article  Google Scholar 

  • Storey, K. B. & J. M. Storey, 1990. Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estimation. Quarterly Review of Biology 65: 145–174.

    Article  CAS  PubMed  Google Scholar 

  • Tamayo, D., 2012. Physiological basis for inter-individual differences in growth among bivalve molluscs. PhD Thesis. University of the Basque Country (UPV/EHU), Bilbao.

  • Tamayo, D., I. Ibarrola & E. Navarro, 2013. Thermal dependence of clearance and metabolic rates in slow- and fast-growing spats of Manila clam Ruditapes philippinarum. Journal of Comparative Physiology B 183: 893–904.

    Article  Google Scholar 

  • Thippeswamy, S. & M. M. Joseph, 1991. Population selection strategies in the wedge clam Donax incarnates (Gmelin) from Panambur beach. Indian Journal of Marine Sciences 20: 147–151.

    Google Scholar 

  • Thippeswamy, S. & M. M. Joseph, 1992. Allometry in the wedge clam Donax incarnates (Gmelin) from Panambur beach. Indian Journal of Marine Sciences 21: 147–149.

    Google Scholar 

  • White, C. R., 2011. Allometric estimation of metabolic rates in animals. Comparative Biochemistry and Physiology Part A 158: 346–357.

    Article  Google Scholar 

  • White, C. R., N. F. Phillips & R. S. Seymour, 2006. The scaling and temperature dependence of vertebrate metabolism. Biology Letters 2: 125–127.

    Article  PubMed  PubMed Central  Google Scholar 

  • Widdows, J., P. Donkin, P. N. Salkeld, J. J. Cleary, D. M. Lowe, S. V. Evans & P. E. Thompson, 1984. Relative importance of environmental factors in determining physiological differences between two populations of mussels (Mytilus edulis). Marine Ecology Progress Series 17: 33–48.

    Article  Google Scholar 

  • Widdows, J. & A. J. S. Hawkins, 1989. Partitioning of rate of heat dissipation by Mytilus edulis into maintenance feeding, and growth components. Physiological Zoology 62: 764–784.

    Article  Google Scholar 

  • Winter, J. E., 1978. A review on the knowledge of suspension-feeding in lamellibranchiate bivalves, with special reference to artificial aquaculture systems. Aquaculture 13: 1–33.

    Article  Google Scholar 

  • Withers, P. C., 1992. Animal Energetics. Comparative Animal Physiology. Saunders College Publishing, Fort Worth: 82–121.

    Google Scholar 

  • Wolowicz, M. & P. Goulletquer, 1999. The shell organic content in the energy budget of Mytilus trossulus from the South Baltic. Haliotis 28: 1–10.

    Google Scholar 

  • Zar, J. H., 1996. Biostatistical Analysis, 3rd ed Prentice-Hall, Englewood Cliffs.

    Google Scholar 

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Acknowledgments

The authors thank Lourdes Nieto and Beatriz González for their expert technical assistance with the algae culture, physiological, and chemical analyses. We thank P. Markaide for his valuable contribution on the custom-made R script. This work was funded by the project FIGEBIV (AGL2013-49144-C3-2-R).

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  1. Consejo Superior de Investigaciones Científicas (CSIC), Instituto de Investigaciones Marinas (IIM), C/Eduardo Cabello 6, 36208, Vigo, Spain

    Kristina Arranz, Uxío Labarta & M. José Fernández-Reiriz

  2. Departamento GAFFA (Animal Physiology), Facultad de Ciencia y Tecnología, Universidad del País Vasco/Euskal Herriko Unibertsitatea, Apartado 644, 48080, Bilbao, Spain

    Enrique Navarro

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  1. Kristina Arranz
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Arranz, K., Labarta, U., Fernández-Reiriz, M.J. et al. Allometric size-scaling of biometric growth parameters and metabolic and excretion rates. A comparative study of intertidal and subtidal populations of mussels (Mytilus galloprovincialis). Hydrobiologia 772, 261–275 (2016). https://doi.org/10.1007/s10750-016-2672-3

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