Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Shifts in shell mineralogy and metabolism of Concholepas concholepas juveniles along the Chilean coast

Laura Ramajo A B F , Alejandro B. Rodríguez-Navarro C , Carlos M. Duarte A D , Marco A. Lardies E and Nelson A. Lagos B
+ Author Affiliations
- Author Affiliations

A Global Change Department, Instituto Mediterráneo de Estudios Avanzados (IMEDEA, CSIC-UIB), C/ Miquel Marqués 21, E-07190 Esporles, Islas Baleares, Spain.

B Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Universidad Santo Tomás, Avenida Ejército 146, 8370003 Santiago, Chile.

C Departamento de Mineralogía y Petrología, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva s/n, 18071 Granada, Spain.

D Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia.

E Facultad de Artes Liberales e Ingeniería y Ciencias, Universidad Adolfo Ibañez, Avenida Diagonal Las Torres 2640, 7041169 Santiago, Chile.

F Corresponding author. Laura Ramajo. Email: lramajo@imedea.uib-csic.es

Marine and Freshwater Research 66(12) 1147-1157 https://doi.org/10.1071/MF14232
Submitted: 5 August 2014  Accepted: 12 January 2015   Published: 7 May 2015

Abstract

Along the west coast of South America, from the tropical zone to the Patagonian waters, there is a significant latitudinal gradient in seawater temperature, salinity and carbonate chemistry. These physical–chemical changes in seawater induce morphological and physiological responses in calcifying organisms, which may alter their energy budget and calcification processes. In this study, we study the organism energy maintenance (i.e. metabolic rate) and mineralogical composition of the shell of the juvenile marine snails Concholepas concholepas (Gastropoda: Muricidae), collected from benthic populations located ~2000 km apart, varies across geographic regions along the Chilean coast. We found that in juvenile snails, the calcite : aragonite ratio in the pallial shell margin (i.e. newly deposited shell) increase significantly from northern to southern populations and this increase in calcite precipitation in the shell of juveniles snails was associated with a decrease in oxygen consumption rates in these populations. Our result suggests that calcite secretion may be favoured when metabolic rates are lowered, as this carbonate mineral phase might be less energetically costly for the organism to precipitate. This result is discussed in relation to the natural process such as coastal upwelling and freshwater inputs that promote geographic variation in levels of pH and carbonate saturation state in seawater along the Chilean coast.

Additional keywords: calcium carbonate, metabolism, ocean acidification, temperature.


References

Addadi, L., and Weiner, S. (1992). Control and design principles in biological mineralization. Angewandte Chemie 31, 153–169.
Control and design principles in biological mineralization.CrossRef |

Bambach, R. K., Knoll, A. H., and Sepkoski, J. J. (2002). Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm. Proceedings of the National Academy of Sciences of the United States of America 99, 6854–6859.
Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm.CrossRef | 1:CAS:528:DC%2BD38XjvFCruro%3D&md5=d6c18465517471f0c31beee4271a1e9cCAS | 12011444PubMed |

Barton, A., Hales, B., Waldbusser, G. G., Langdon, C., and Feely, R. A. (2012). The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: implications for near-term ocean acidification effects. Limnology and Oceanography 57, 698–710.
The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: implications for near-term ocean acidification effects.CrossRef | 1:CAS:528:DC%2BC38XhtVOmtrfI&md5=3c7370d9e351071e3ffadea781ac9676CAS |

Belcher, A., Wu, X., Christensen, R., Hansma, P., Stucky, G., and Morse, D. (1996). Control of crystal phase switching and orientation by soluble mollusc shell proteins. Nature 381, 56–58.
Control of crystal phase switching and orientation by soluble mollusc shell proteins.CrossRef | 1:CAS:528:DyaK28XislCrurY%3D&md5=3070584707ebf0a8f2c2a880a50aee7aCAS |

Bertram, M. A., Mackenzie, M. A., Bishop, F. T., and Bischoff, W. D. (1991). Influence of temperature on the stability of magnesian calcite. The American Mineralogist 76, 108–134.

Bøggild, O. B. (1930). The shell structure of the Mollusks. Det Kongelige Danske videnskabernes selskabs skrifter, Naturvidenskabelig og mathematisk afdeling 9, 231–326.

Burton, E. A., and Walter, L. M. (1987). Relative precipitation rates of aragonite and Mg-calcite from seawater: temperature or carbonate ion control? Geology 15, 111–114.
Relative precipitation rates of aragonite and Mg-calcite from seawater: temperature or carbonate ion control?CrossRef | 1:CAS:528:DyaL2sXhvVSisLY%3D&md5=6737550650bda2e8d225e4deab117d2fCAS |

Burton, E. A., and Walter, L. M. (1991). The effects of pCO2 and temperature on magnesium incorporation in calcite in seawater and MgCl2–CaCl2 solutions. Geochimica et Cosmochimica Acta 55, 777–785.
The effects of pCO2 and temperature on magnesium incorporation in calcite in seawater and MgCl2–CaCl2 solutions.CrossRef |

Byrne, M. (2011). Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanography and Marine Biology – an Annual Review 49, 1–42.

Cohen, A. L., and Branch, G. M. (1992). Environmentally controlled variation in the structure and mineralogy of Patella granularis shells from the coast of southern Africa: implications for paleotemperature assessments. Palaeogeography, Palaeoclimatology, Palaeoecology 91, 49–57.
Environmentally controlled variation in the structure and mineralogy of Patella granularis shells from the coast of southern Africa: implications for paleotemperature assessments.CrossRef |

Comeau, S., Gorsky, G., Jeffree, R., Teyssié, J. L., and Gattuso, J. P. (2009). Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina). Biogeosciences 6, 1877–1882.
Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina).CrossRef | 1:CAS:528:DC%2BD1MXhsFWltrzI&md5=cca1cc147ea9e876c6556a0dffc65eb5CAS |

Dauphin, Y., Guzmán, N., Denis, A., Cuif, J. P., and Ortlieb, J. L. (2003). Microstructure, nanostructure and composition of the shell of Concholepas concholepas (Gastropoda, Muricidae). Aquatic Living Resources 16, 95–103.
Microstructure, nanostructure and composition of the shell of Concholepas concholepas (Gastropoda, Muricidae).CrossRef |

Dávila, P. M., Figueroa, D., and Müller, E. (2002). Freshwater input into the coastal ocean and its relation with the salinity distribution off austral Chile (35–55°S). Continental Shelf Research 22, 521–534.
Freshwater input into the coastal ocean and its relation with the salinity distribution off austral Chile (35–55°S).CrossRef |

Dickson, J. A. D. (2004). Echinoderm skeletal preservation: calcite–aragonite seas and the Mg/Ca ratio of Phanerozoic oceans. Journal of Sedimentary Research 74, 355–365.
Echinoderm skeletal preservation: calcite–aragonite seas and the Mg/Ca ratio of Phanerozoic oceans.CrossRef | 1:CAS:528:DC%2BD2cXkslOktLs%3D&md5=c759dae1458c51696ed5886724072846CAS |

Dodd, J. R. (1963). Paleoecological implications of shell mineralogy in two pelecypod species. The Journal of Geology 71, 1–11.
Paleoecological implications of shell mineralogy in two pelecypod species.CrossRef |

Dodd, J. R. (1964). Environmentally controlled variation in the shell structure of a pelecypod species. Paleontological Journal 38, 1065–1071.

Dodd, J. R. (1966). The influence of salinity on mollusk shell mineralogy: a discussion. The Journal of Geology 74, 85–89.
The influence of salinity on mollusk shell mineralogy: a discussion.CrossRef |

Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. (2009). Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169–192.
Ocean acidification: the other CO2 problem.CrossRef | 21141034PubMed |

Duarte, C. M., Hendriks, I. E., Moore, T. S., Olsen, Y. S., Steckbauer, A., Ramajo, L., Carstensen, J., Trotter, J. A., and McCulloch, M. (2013). Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on marine pH. Estuaries and Coasts 36, 221–236.
Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on marine pH.CrossRef | 1:CAS:528:DC%2BC3sXjvVKmu74%3D&md5=4ec80fea4fd5580e93b02b8017ccfc3aCAS |

Dupont, S., Ortega-Martinez, O., and Thorndyke, M. (2010). Impact of near-future ocean acidification on echinoderms. Ecotoxicology (London, England) 19, 449–462.
Impact of near-future ocean acidification on echinoderms.CrossRef | 1:CAS:528:DC%2BC3cXjtVGjsbk%3D&md5=095a115b95dd627912ff7ce95a80916eCAS |

Eisma, D. (1966). The influence of salinity on mollusk shell mineralogy: a discussion. The Journal of Geology 74, 89–94.
The influence of salinity on mollusk shell mineralogy: a discussion.CrossRef |

Fabry, V. J., Seibel, B. A., Feely, R. S., and Orr, J. C. (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. Journal of Marine Science 65, 414–432.
| 1:CAS:528:DC%2BD1cXntFegtL4%3D&md5=51e793d49d48944e0ade5a432c1e3adeCAS |

Gattuso, J. P., and Hansson, L. (2011). Ocean acidification: background and history. In ’Ocean acidification’. (Eds J. P. Gattuso and L. Hansson.) pp. 1–20. (Oxford University Press: Oxford, UK.)

Goffredo, S., Prada, F., Caroselli, E., Capaccioni, B., Zaccanti, F., Pasquini, L., Fantazzini, P., Fermani, S., Reggi, M., Levy, O., Fabricius, K. E., Dubinsky, Z., and Falini, G. (2014). Biomineralization control related to population density under ocean acidification. Nature Climate Change 4, 593–597.
Biomineralization control related to population density under ocean acidification.CrossRef | 1:CAS:528:DC%2BC2cXos1akurg%3D&md5=507efbf554b733965cc307cce6fa01f9CAS | 25071869PubMed |

Green, M. A., Jones, M. E., Boudreau, C. L., Moore, R. L., and Westman, B. A. (2004). Dissolution mortality of juvenile bivalves in coastal marine deposits. Limnology and Oceanography 49, 727–734.
Dissolution mortality of juvenile bivalves in coastal marine deposits.CrossRef |

Gutowska, M. A., Melzner, F., Pörtner, H. O., and Meier, S. (2010). Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis. Marine Biology 157, 1653–1663.
Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis.CrossRef | 1:CAS:528:DC%2BC3cXns1Shs7w%3D&md5=6357989a33e007501261180a9367d8c0CAS |

Guzmán, N. (2004). Validation d’une approche scléroclimatologique sur la côte du Chili et du Pérou par l’analyse microstructurale et biogéochimique des coquilles du gastéropode Concholepas concholepas [Bruguière, 1989]. Ph.D. Thesis, Universite de Paris-Sud.

Guzmán, N., Dauphin, Y., Cuif, J. P., Denis, A., and Ortlieb, L. (2009). Diagenetic changes in Concholepas concholepas shells (Gastropoda, Muricidae) in the hyper-arid conditions on Northern Chile – implications for palaeoenvironmetal reconstructions. Biogeosciences 6, 197–207.
Diagenetic changes in Concholepas concholepas shells (Gastropoda, Muricidae) in the hyper-arid conditions on Northern Chile – implications for palaeoenvironmetal reconstructions.CrossRef |

Hale, R., Calosi, P., McNeill, L., Mieszkowska, N., and Widdicombe, S. (2011). Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120, 661–674.
Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities.CrossRef |

Harper, E. M. (2000). Are calcitic layers and effective adaptation against shell dissolution in the Bivalvia? Journal of Zoology 251, 179–186.
Are calcitic layers and effective adaptation against shell dissolution in the Bivalvia?CrossRef |

Harper, E. M., Palmer, T. J., and Alphey, J. R. (1997). Evolutionary response by bivalves to changing Phanerozoic sea-water chemistry. Geological Magazine 134, 403–407.
Evolutionary response by bivalves to changing Phanerozoic sea-water chemistry.CrossRef |

Hautmann, M. (2006). Shell mineralogical trends in epifaunal Mesozoic bivalves and their relationship to seawater chemistry and atmospheric carbon dioxide concentration. Facies 52, 417–433.
Shell mineralogical trends in epifaunal Mesozoic bivalves and their relationship to seawater chemistry and atmospheric carbon dioxide concentration.CrossRef |

Hendriks, I. E., Duarte, C. M., and Alvarez, M. (2010). Vulnerability of marine biodiversity to ocean acidification; a meta-analysis. Estuarine, Coastal and Shelf Science 86, 157–164.
Vulnerability of marine biodiversity to ocean acidification; a meta-analysis.CrossRef | 1:CAS:528:DC%2BD1MXhs1aqtbvM&md5=46fde8894a127e160f4b10f053c4c2e8CAS |

Hendriks, I. E., Duarte, C. M., Olsen, Y. S., Steckbauer, A., Ramajo, L., Moore, T. S., Trotter, J. A., and McCulloch, M. (2015). Biological mechanisms supporting adaptation to ocean acidification in coastal ecosystems. Estuarine, Coastal and Shelf Science 152, A1–A8.
Biological mechanisms supporting adaptation to ocean acidification in coastal ecosystems.CrossRef | 1:CAS:528:DC%2BC2cXhtlOmt7jE&md5=ca89bf5d280ce9449d366cd36392b9e3CAS |

Hubbard, F., McManus, J., and Al-Dabbas, M. (1981). Environmental influences on the shell mineralogy of Mytilus edulis. Geo-Marine Letters 1, 267–269.
Environmental influences on the shell mineralogy of Mytilus edulis.CrossRef |

Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L., Singh, G. S., Duarte, C. M., and Gattuso, J. P. (2013). Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19, 1884–1896.
Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming.CrossRef | 23505245PubMed |

Lagos, N. A., Navarrete, S. A., Véliz, F., Masuero, A., and Castilla, J. C. (2005). Meso-scale spatial variation in settlement and recruitment of intertidal barnacles along central Chile. Marine Ecology Progress Series 290, 165–178.
Meso-scale spatial variation in settlement and recruitment of intertidal barnacles along central Chile.CrossRef |

Lagos, N. A., Castilla, J. C., and Broitman, B. R. (2008). Spatial environmental correlates of intertidal recruitment: a test using barnacles in northern Chile. Ecological Monographs 78, 245–261.
Spatial environmental correlates of intertidal recruitment: a test using barnacles in northern Chile.CrossRef |

Langenbuch, M., and Pörtner, H. O. (2002). Changes in metabolic rate and N excretion in the marine invertebrate Sipunculus nudus under conditions of environmental hypercapnia: identifying effective acid–base variables. The Journal of Experimental Biology 205, 1153–1160.
| 1:CAS:528:DC%2BD38XktF2qsbY%3D&md5=36120ac4785115088d38378993745af5CAS | 11919274PubMed |

Lannig, G., Eilers, S., Pörtner, H. O., Sokolova, I. A., and Bock, C. (2010). Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas. Changes in metabolic pathways and thermal response. Marine Drugs 8, 2318–2339.
Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas. Changes in metabolic pathways and thermal response.CrossRef | 1:CAS:528:DC%2BC3cXhtVGnsb3I&md5=bafb39fa7141b3b17706d742d13c4963CAS | 20948910PubMed |

Lardies, M. A., and Castilla, J. C. (2001). Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodes chilensis (Decapoda:Pinotheridae) along the Chilean coast. Marine Biology 139, 1125–1133.
Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodes chilensis (Decapoda:Pinotheridae) along the Chilean coast.CrossRef |

Lardies, M. A., Naya, D. E., and Bozinovic, F. (2008). The cost of living slowly: metabolism, Q10 and repeatability in a South American harvestman. Physiological Entomology 33, 193–199.
The cost of living slowly: metabolism, Q10 and repeatability in a South American harvestman.CrossRef | 1:CAS:528:DC%2BD1cXhtF2mtL3P&md5=fd0c4301250f175e48bc8e09da1e0316CAS |

Lardies, M. A., Muñoz, J. L., Paschke, K. A., and Bozinovic, F. (2011). Latitudinal variation in the aerial/aquatic ratio of oxygen consumption of a supratidal high rocky-shore crab. Marine Ecology (Berlin) 32, 42–51.
Latitudinal variation in the aerial/aquatic ratio of oxygen consumption of a supratidal high rocky-shore crab.CrossRef | 1:CAS:528:DC%2BC3MXjs12rsrw%3D&md5=0c8bebc3e334ef120a0eacb7be9fadc1CAS |

Lardies, M. A., Arias, M. B., Poupin, M. J., Manríquez, P. H., Torres, R., Vargas, C. A., Navarro, J. M., and Lagos, N. A. (2014). Differential response to ocean acidification in physiological traits of Concholepas concholepas populations. Journal of Sea Research 90, 127–134.
Differential response to ocean acidification in physiological traits of Concholepas concholepas populations.CrossRef |

Lefèvre, N., Aiken, J., Rutllant, J., Daneri, G., Lavender, S., and Smyth, T. (2002). Observations of pCO2 in the coastal upwelling off Chile: spatial and temporal extrapolation using satellite data. Journal of Geophysical Research 107, 3055.
Observations of pCO2 in the coastal upwelling off Chile: spatial and temporal extrapolation using satellite data.CrossRef |

Lowenstam, H. (1954a). Environmental relations of modification compositions of certain carbonate secreting marine invertebrates. Proceedings of the National Academy of Sciences of the United States of America 40, 39–48.
Environmental relations of modification compositions of certain carbonate secreting marine invertebrates.CrossRef | 1:CAS:528:DyaG2cXkslCrsw%3D%3D&md5=fa263e9be040c4c628be80e102c6fafdCAS | 16589423PubMed |

Lowenstam, H. (1954b). Factors affecting the aragonite-calcite ratios in carbonate-secreting marine organisms. The Journal of Geology 62, 284–322.
Factors affecting the aragonite-calcite ratios in carbonate-secreting marine organisms.CrossRef | 1:CAS:528:DyaG2cXksF2kug%3D%3D&md5=fdc864f0b765f944b0d672204a98c57fCAS |

Malone, P. G., and Dodd, J. R. (1967). Temperature and salinity effects on calcification rate in Mytilus edulis and its paleoecological implications. Limnology and Oceanography 12, 432–436.
Temperature and salinity effects on calcification rate in Mytilus edulis and its paleoecological implications.CrossRef | 1:CAS:528:DyaF2sXltFCltr8%3D&md5=b0b363640b4f46fece9a67740e419aa2CAS |

Manríquez, P. H., Delgado, A. P., Jara, M. E., and Castilla, J. C. (2008). Field and laboratory experiments with early ontogenetic stages of Concholepas concholepas under field and laboratory conditions in Central Chile. Aquaculture 279, 99–107.
Field and laboratory experiments with early ontogenetic stages of Concholepas concholepas under field and laboratory conditions in Central Chile.CrossRef |

Mayol, E., Ruiz-Halpern, S., Duarte, C. M., Castilla, J. C., and Pelegrí, J. L. (2012). Coupled CO2 and O2-driven compromises to marine life in summer along the Chilean sector of the Humboldt Current System. Biogeosciences 9, 1183–1194.
Coupled CO2 and O2-driven compromises to marine life in summer along the Chilean sector of the Humboldt Current System.CrossRef | 1:CAS:528:DC%2BC38Xhs1Gks73E&md5=c661916c613d830064b55203f7101d0bCAS |

McClintock, J. B., Angus, R. A., Mcdonald, M. R., Amsler, C. D., Catledge, S. A., and Vohra, Y. K. (2009). Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification. Antarctic Science 21, 449–456.
Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification.CrossRef |

Michaelidis, B., Ouzounis, C., Paleras, A., and Pörtner, H. O. (2005). Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 293, 109–118.
Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis.CrossRef |

Morse, J. W., Wang, Q., and Tsio, M. Y. (1997). Influences of temperature and Mg:Ca ratio on CaCO3 precipitates from seawater. Geology 25, 85–87.
Influences of temperature and Mg:Ca ratio on CaCO3 precipitates from seawater.CrossRef | 1:CAS:528:DyaK2sXht1Srt70%3D&md5=d56bdacc6328dc3e004d63a9a88711faCAS |

Mucci, A. (1987). Influence of temperature on the composition of magnesian calcite overgrowths precipitated from seawater. Geochimica et Cosmochimica Acta 51, 1977–1984.
Influence of temperature on the composition of magnesian calcite overgrowths precipitated from seawater.CrossRef | 1:CAS:528:DyaL2sXltFygu7s%3D&md5=87a05f54e20852e04788c480b5c031b7CAS |

Ogino, T., Suzuki, T., and Sawada, K. (1987). The formation and transformation mechanism of calcium carbonate in water. Geochimica et Cosmochimica Acta 51, 2757–2767.
The formation and transformation mechanism of calcium carbonate in water.CrossRef | 1:CAS:528:DyaL1cXkslSluw%3D%3D&md5=d0194f082d6a9987a22fa59eaa0d80e8CAS |

Osovitz, C. J., and Hofmann, G. E. (2007). Marine macrophysiology: studying physiological variation across large spatial scales in marine systems. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 147, 821–827.
Marine macrophysiology: studying physiological variation across large spatial scales in marine systems.CrossRef |

Paine, R. T. (1971). A short-term experimental investigation of resource partitioning in a New Zealand rocky intertidal habitat. Ecology 52, 1096–1106.
A short-term experimental investigation of resource partitioning in a New Zealand rocky intertidal habitat.CrossRef |

Palmer, A. R. (1983). Relative cost of producing skeletal organic matrix versus calcification: evidence from marine gastropods. Marine Biology 75, 287–292.
Relative cost of producing skeletal organic matrix versus calcification: evidence from marine gastropods.CrossRef |

Palmer, A. R. (1992). Calcification in marine mollusks: how costly is it? Proceedings of the National Academy of Sciences of the United States of America 89, 1379–1382.
Calcification in marine mollusks: how costly is it?CrossRef | 1:CAS:528:DyaK38XhsVymu7w%3D&md5=6065ce28a155a8793ac450211dad11c4CAS | 11607278PubMed |

Putnis, A., Prieto, M., and Fernández-Diaz, L. (1995). Fluid supersaturation and crystallization in porous-media. Geological Magazine 132, 1–13.
Fluid supersaturation and crystallization in porous-media.CrossRef | 1:CAS:528:DyaK2MXktlamur4%3D&md5=3d098bff957a71b19e187b8a664ea8cdCAS |

R Development Core Team (2009). R: a language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org [Verified 26 June 2012].

Radishi, N. A., Mohamed, M., and Yusup, S. (2012). The kinetic model of calcination and carbonation of Anadara Granosa. Renewable Energy 2, 497–503.

Ramajo, L., Baltanás, A., Torres, R., Manríquez, P. H., and Lagos, N. A. (2013). Geographic variation in shell morphology, weight and mineralization of juvenile snails of Concholepas concholepas (loco) along the Chilean coast. Journal of the Marine Biological Association of the United Kingdom 93, 2167–2176.
Geographic variation in shell morphology, weight and mineralization of juvenile snails of Concholepas concholepas (loco) along the Chilean coast.CrossRef | 1:CAS:528:DC%2BC3sXhslCgu7vF&md5=6beabee41f8c5a0e934d99b1026d98e4CAS |

Ries, J. B. (2011). Skeletal mineralogy in a high-CO2 world. Journal of Experimental Marine Biology and Ecology 403, 54–64.
Skeletal mineralogy in a high-CO2 world.CrossRef | 1:CAS:528:DC%2BC3MXmtVyit7w%3D&md5=e796ab90253035f0bccb40b5f415d780CAS |

Rodríguez-Navarro, A., CabraldeMelo, C., Batista, N., Morimoto, N., Alvarez-Lloret, P., Ortega-Huertas, M., Fuenzalida, V. M., Arias, J. I., Wiff, J. P., and Arias, J. L. (2006). Microstructure and crystallographic-texture of giant barnacle (Austromegabalanus psittacus) shell. Journal of Structural Biology 156, 355–362.
Microstructure and crystallographic-texture of giant barnacle (Austromegabalanus psittacus) shell.CrossRef | 16962792PubMed |

Saleuddin, A. S. M., and Kunigelis, S. C. (1984). Neuroendocrine control mechanism in shell formation. American Zoologist 24, 9111–9116.

Salisbury, J., Green, M., Hunt, C., and Campbell, J. (2008). Coastal acidification by rivers: a new threat to shellfish. Eos, Transactions, American Geophysical Union 89, 513.
Coastal acidification by rivers: a new threat to shellfish.CrossRef |

Schifano, G. (1982). Temperature effects on shell mineralogy and morphology in three gastropod species. Marine Geology 45, 79–91.
Temperature effects on shell mineralogy and morphology in three gastropod species.CrossRef |

Simkiss, K., and Wilbur, K. M. (1989). ‘Biomineralization: Cell Biology and Mineral Deposition.’ (Academic Press: San Diego, CA.)

Storch, D., Fernández, M., Navarette, S., and Pörtner, H. (2011). Thermal tolerance of larval stages of the Chilean kelp crab Taliepus dentatus. Marine Ecology Progress Series 429, 157–167.
Thermal tolerance of larval stages of the Chilean kelp crab Taliepus dentatus.CrossRef |

Strub, T., Mesías, J., Montecino, V., Rutllant, J., and Salinas, S. (1998). Coastal ocean circulation off western South America. Coastal segment. In ‘The Sea’. (Eds A. R. Robinson and K. H. Brink.) pp. 273–313. (Wiley: Hoboken, NJ, USA.)

Stumpp, M., Wren, J., Melzner, F., Thorndyke, M. C., and Dupont, S. T. (2011). Seawater acidification impacts sea urchin larval development. I. Elevated metabolic rates decrease scope for growth and induce developmental delay. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 160, 331–340.
Seawater acidification impacts sea urchin larval development. I. Elevated metabolic rates decrease scope for growth and induce developmental delay.CrossRef | 1:CAS:528:DC%2BC3MXhtV2ntL7O&md5=2e50c9c6d37bbf476337441ef511a817CAS |

Taylor, J. D. (1973). The structural evolution of the bivalve shell. Palaeontology 16, 519–534.

Taylor, J. D., and Layman, M. A. (1972). The mechanical properties of bivalve (Mollusca) shell structure. Palaeontology 15, 73–87.

Taylor, J. D., Kennedy, W., and Hall, A. (1969). Shell structure and mineralogy of the Bivalvia. Introduction. Nuculacae-Trigonacae. Bulletin of the British Museum (Natural History). Zoology 3, 1–125.

Torres, R., Turner, D., Rutlant, J., Sobarzo, M., Antezana, T., and Gonzalez, H. (2002). CO2 outgassing off Central Chile (31–30°S) and northern Chile (24–23°S) during austral summer 1997: the effect of wind intensity on the upwelling and ventilation of CO2-rich waters. Deep-sea Research. Part I, Oceanographic Research Papers 49, 1413–1429.
CO2 outgassing off Central Chile (31–30°S) and northern Chile (24–23°S) during austral summer 1997: the effect of wind intensity on the upwelling and ventilation of CO2-rich waters.CrossRef | 1:CAS:528:DC%2BD38XmtlWgtbY%3D&md5=d438a57deaca97677026e12661b983e4CAS |

Torres, R., Pantoja, S., Harada, N., González, H. E., Daneri, G., Frangopulos, M., Rutllant, J. A., Duarte, C. M., Rúiz-Halpern, S., Mayol, E., and Fukasawa, M. (2011). Air–sea CO2 fluxes along the coast of Chile: from CO2 outgassing in central–northern upwelling waters to CO2 sequestering in southern Patagonian fjords. Journal of Geophysical Research 116, .
Air–sea CO2 fluxes along the coast of Chile: from CO2 outgassing in central–northern upwelling waters to CO2 sequestering in southern Patagonian fjords.CrossRef | 1:CAS:528:DC%2BC38XoslCnsLw%3D&md5=0f77df34c0dafbcf04d8ddf5519e41f6CAS |

Vernberg, F. J. (1959). Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. II. Oxygen consumption of whole organisms. The Biological Bulletin 117, 163–184.
Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca. II. Oxygen consumption of whole organisms.CrossRef | 1:CAS:528:DyaF3cXlvVSmuw%3D%3D&md5=511e95d1db73fb44fb2a27a1b581b24aCAS |

Vernberg, F. J., and Vernberg, W. B. (1964). Metabolic adaptation of animals from different latitudes. Helgoland Marine Research 9, 476–487.

Waldbusser, G. G., and Salisbury, J. E. (2014). Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains, and habitats. Annual Review of Marine Science 6, 221–247.
Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains, and habitats.CrossRef | 23987912PubMed |

Waldbusser, G. G., Bergschneider, H., and Green, M. A. (2010). Size-dependent pH effect on calcification in post-larval hard clam Mercenaria spp. Marine Ecology Progress Series 417, 171–182.
Size-dependent pH effect on calcification in post-larval hard clam Mercenaria spp.CrossRef |

Waldbusser, G. G., Steenson, R. A., and Green, M. A. (2011). Oyster shell dissolution rates in estuarine waters: effects of pH and shell legacy. Journal of Shellfish Research 30, 659–669.
Oyster shell dissolution rates in estuarine waters: effects of pH and shell legacy.CrossRef |

Waldbusser, G. G., Brunner, E. L., Haley, B. A., Hales, B., Langdon, C. J., and Prahl, F. G. (2013). A developmental and energetic basis linking larval oyster shell formation to ocean acidification. Geophysical Research Letters 40, 2171–2176.
A developmental and energetic basis linking larval oyster shell formation to ocean acidification.CrossRef | 1:CAS:528:DC%2BC3sXhtVaru77K&md5=267a4e36572e0964d39dc36cf5fd12e5CAS |

Walter, L. M. (1986) Relative efficiency of carbonate dissolution and precipitation during diagenesis: a progress report on the role of solution chemistry. In ‘Roles of Organic Matter in Sediment Diagenesis’. (Eds D. L. Gautier.) Special Publication 38, pp. 1–11 (Society of Economic Paleontologics and Mineralogists: Tulsa, OK, USA.)

Watabe, N., and Wilbur, K. (1960). Influence of the organic matrix on crystal type in mollusks. Nature 188, 334.
Influence of the organic matrix on crystal type in mollusks.CrossRef |

Welladsen, H. M., Southgate, P. C., and Heimann, K. (2010). The effects of exposure to near-future levels of ocean acidification on shell characteristics of Pinctada fucata (Bivalvia: Pteriidae). Molluscan Research 30, 125–130.

Whiteley, N. M., Taylor, E. W., and El-Haj, A. J. (1997). Seasonal and latitudinal adaptation to temperature in crustaceans. Journal of Thermal Biology 22, 419–427.
Seasonal and latitudinal adaptation to temperature in crustaceans.CrossRef |

Yamamoto-Kawai, M., McLaughlin, F., Carmack, E. C., Nishino, S., and Shimada, K. (2009). Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt. Science 326, 1098–1100.
Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt.CrossRef | 1:CAS:528:DC%2BD1MXhsVentLvO&md5=78d212dd13ad0aceb7799b1da83b2a5aCAS | 19965425PubMed |

Zeller, E. J., and Wray, J. L. (1956). Factors influencing the precipitation of calcium carbonate. The American Association of Petroleum Geologists Bulletin 40, 140–152.

Zhong, S., and Mucci, A. (1989). Calcite and aragonite precipitation from seawater solutions of various salinities: precipitation rates and overgrowth compositions. Chemical Geology 78, 283–299.
Calcite and aragonite precipitation from seawater solutions of various salinities: precipitation rates and overgrowth compositions.CrossRef | 1:CAS:528:DyaK3cXhsVarurY%3D&md5=13616b5dd1846f2bcc0e5dfd79d3e3e0CAS |



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