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Estuaries and Coasts

, Volume 38, Issue 2, pp 590–598 | Cite as

Intraspecific Variability in the Response of the Edible Mussel Mytilus chilensis (Hupe) to Ocean Acidification

  • Cristian Duarte
  • Jorge M. Navarro
  • Karin Acuña
  • Rodrigo Torres
  • Patricio H. Manríquez
  • Marcos A. Lardies
  • Cristian A. Vargas
  • Nelson A. Lagos
  • Víctor Aguilera
Article

Abstract

Ocean acidification (OA) has been shown to affect significantly the net calcification process and growth rate of many marine calcifying organisms. Recent studies have shown that the responses of these organisms to OA can vary significantly among species. However, much less is known concerning the intraspecific variability in response to OA. In this study, we compared simultaneously the responses of two populations of the edible mussel Mytilus chilensis (Hupe) exposed to OA. Three nominal CO2 concentrations (380, 700, and 1,000 μatm of CO2) were used. Negative effects of CO2 increase on net calcification rate were only found in individuals from Huelmo Bay. However, no effects were found in individuals from Yaldad Bay. Moreover, OA had not significant effects on the shell dissolution rate in individuals from both localities. This suggests that the negative effect of the OA on the net calcification rate of this species is explained by shell deposition, but not by the shell dissolution processes. We do not know the specific underlying mechanisms responsible for these differences, but some possibilities are discussed. These results highlight that the responses of marine organism to OA can be highly variable even within the same species. Therefore, more studies across the distribution range of the species, considering environmental variability, are needed for a better understanding of the consequences of OA on marine organisms. Finally, because mussels exert influence on their physical and biological surroundings, the negative effects of a CO2 increase could have significant ecological consequences.

Keywords

Ocean acidification Mussel Calcification Growth rate 

Notes

Acknowledgments

The authors are grateful to Jorge López, Bárbara Cisternas, María Elisa Jara, and Loreto Mardones for their valuable assistance during the experiments and for the algae production. The manuscript was improved thanks to the comments from three anonymous reviewers. Financial support provided by the Programa de Investigación Asociativa, PIA-CONICYT-CHILE (Grant Anillos ACT-132) is gratefully acknowledged. This is Anillos ACT-132 publication no. 9. This study was also partially funded by Project Fondecyt no. 11110407 (to CD). The Millennium Scientific 13 Initiative Grant IC120019 also supported this work during the final stage. CAV is supported by Red 14 Doctoral REDOC.CTA, MINEDUC project UCO1202 at U. de Concepción.

References

  1. Arnold, K.E., H.S. Findlay, J.I. Spicer, C.L. Daniels, and D. Boothroyd. 2009. Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences Discuss 6: 3087–3107.CrossRefGoogle Scholar
  2. Beniash, E., A. Ivanina, N.S. Lieb, I. Kurochkin, and I.M. Sokolova. 2010. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Marien Ecolgy Progress Series 419: 95–108.CrossRefGoogle Scholar
  3. Berge, J.A., B. Bjerkeng, O. Pettersen, M.T. Schaanning, and S. Oxnevad. 2006. Effects of increased sea water concentrations of CO2 on growth of the bivalve Mytilus edulis L. Chemosphere 62: 681–687.CrossRefGoogle Scholar
  4. Cáceres, M., A. Valle-Levinson, and M. Bello. 2008. Residual flow over a bump in Quellón Bay. Revista de Biología Marina y Oceanografía 43: 629–639.CrossRefGoogle Scholar
  5. Cai, W-J., X. Hu, W-J. Huang, M.C. Murrell, J.C. Lehrter, S.E. Lohrenz, W-Ch. Chou, W. Zhai, J.T. Hollibaugh, Y. Wang, P. Zhao, X. Guo, K. Gundersen, M. Dai and G-Ch. Gong. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4: 766–770Google Scholar
  6. Caldeira, K., and M.E. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425: 365.CrossRefGoogle Scholar
  7. Cummings, V., J. Hewitt, A. Van Rooyen, K. Currie, S. Beard, S. Thrush, J. Norkko, N. Barr, P. Heath, N.J. Halliday, R. Sedcole, A. Gomez, C. McGraw, and V. Metcalf. 2011. Ocean acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica. PLoS ONE 6(1): e16069.CrossRefGoogle Scholar
  8. Dickson, A.G., and F.J. Millero. 1987. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research 34(10A): 1733–1743.CrossRefGoogle Scholar
  9. DOE. 1994. Handbook of methods for the analysis of the various parameters of the carbon dioxide system in sea water; version 2, Dickson, A.G., Goyet, C., (Eds.), ORNL/CDIAC, 74.Google Scholar
  10. Doney, S.C., V.J. Fabry, R.A. Feely, and J.A. Kleypas. 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1(1): 169–192.CrossRefGoogle Scholar
  11. Duarte, C., E. Jaramillo, H. Contreras, and L. Figueroa. 2006. Community structure of the macroinfauna in the sediments below and intertidal mussel bed (Mytilus chilensis)(Hupe) of southern Chile. Revista Chilena de Historia Natural 79: 353–368.CrossRefGoogle Scholar
  12. Duarte, C., J.M. Navarro, K. Acuña, R. Torres, P.H. Manríquez, M.A. Lardies, C.A. Vargas, N.A. Lagos, and V. Aguilera. 2014. Combined effects of temperature and ocean acidification on the juvenile individuals of the mussel Mytilus chilensis. Journal of Sea Research 85: 308–314.CrossRefGoogle Scholar
  13. Fabry, V.J., B.A. Seibel, R.A. Feely, and J.C. Orr. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65: 414–432.CrossRefGoogle Scholar
  14. Feely, R.A., C.L. Sabine, J.M. Hernandez-Ayon, D. Ianson, and B. Hales. 2008. Evidence for upwelling of corrosive “acidified” water onto the continental shelf science 320: 1490Google Scholar
  15. Findlay, H.S., M.A. Kendall, J.I. Spicer, and S. Widdicombe. 2009. Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Marine Biology. doi: 10.1007/s00227-009-1356-1.Google Scholar
  16. Gazeau, F., C. Quiblier, J. Jansen, J.P. Gattuso, J. Middleburg, and C. Heip. 2007. Impact of elevated CO2 on shellfish calcification. Geophysical Research Letters 34: 1–15.CrossRefGoogle Scholar
  17. Gazeau, F., J.-P. Gattuso, C. Dawber, A.E. Pronker, F. Peene, J. Peene, C.H.R. Heip, and J.J. Middelburg. 2010. Effect of ocean acidification on the early life stages of the blue mussel (Mytilus edulis). Biogeoscience Discuss 7: 2927–2947.CrossRefGoogle Scholar
  18. Gooding, R.A., C.D.G. Harley, and E. Tang. 2009. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proceeding of the National Academy of Science 106: 9316–9321.CrossRefGoogle Scholar
  19. Gutowska, M.A., H.O. Pörtner, and F. Melzner. 2008. Growth and calcification in the cephalopod Sepia officinalis under elevated seawater pCO2. Marine Ecology Progress Series 373: 303–309.CrossRefGoogle Scholar
  20. Gutowska, M.A., F. Melzner, M. Langenbuch, C. Bock, G. Claireaux, and H.O. Pörtner. 2010. Acid–base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. Journal of Comparative Physiology B 180: 323–335.CrossRefGoogle Scholar
  21. Hall-Spencer, J.M., R. Rodolfo-Metalpa, S. Martin, E. Ransome, M. Fine, S.M. Turner, S.J. Rowley, D. Tedesco, and M.-C. Buia. 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96–99.CrossRefGoogle Scholar
  22. Haraldsson, C., L.G. Anderson, M. Hassellöv, S. Hulth, and K. Olsson. 1997. Rapid, high-precision potentiometric titration of alkalinity in ocean and sediment pore waters. Deep-Sea Res. Part I: Oceanographic Research Papers 44(12): 2031–2044.Google Scholar
  23. Havenhand, J.N., and P. Schlegel. 2009. Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences 6: 3009–3015.CrossRefGoogle Scholar
  24. Hiebenthal, C., E.E.R. Philipp, A. Eisenhauer, and M. Wahl. 2013. Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.). Marine Biology 160: 2073–2087.CrossRefGoogle Scholar
  25. Houghton, J.T., L.G. Meira Filho, B.A. Callander, N. Harris, A. Kattenberg, and K. Maskell. 1996. Climate Change 1995, The science of climatic change, 572. Cambridge: Cambridge University.Google Scholar
  26. Houghton, J.T., Y. Ding, D.J. Griggs, M. Noguer, M. Van der Linden, X. Dai, K. Maskell, and C.A. Johnson. 2001. Climate change 2001: the scientific basis (Contribution of WG1 to the IPCC Third Assessment). Cambridge: University Cambridge.Google Scholar
  27. Iglesias-Rodriguez, M.D., P.R. Halloran, R.E.M. Rickaby, I.R. Hall, E. Colmenero-Hidalgo, J.R. Gittins, D.R.H. Green, T. Tyrrell, S.J. Gibbs, P. Von Dassow, E. Rehm, E.V. Armbrust, and K.P. Boessenkool. 2008. Phytoplankton calcification in a high-CO2 world. Science 320: 336–340.CrossRefGoogle Scholar
  28. Ilyina, T., R.E. Zeebe, E. Maier-Reimer, and C. Heinze. 2009. Early detection of ocean acidification effects on marine calcification. Global Biogeochemical Cycles 23, GB1008.CrossRefGoogle Scholar
  29. IPCC: Climate Change, 2007. The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment, Report of the Intergovernmental Panel on Climate Change. In: Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, H.L. Miller, (Eds.), Cambridge University, Cambridge, UK, p. 996.Google Scholar
  30. Kleypas, J.A., R.A. Feely, V.J. Fabry, C. Langdon, C.L. Sabine, and L.L. Robbins. 2006. Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research, report of a workshop held 18–20 April (2005), St. Petersburg, FL, sponsored by NSF, NOAA, and the US Geological Survey.Google Scholar
  31. Krapivka, S., J.E. Toro, A.C. Alcapan, M. Astorga, P. Presa, M. Perez, and R. Guinez. 2007. Shell-shape variation along the latitudinal range of the Chilean blue mussel Mytilus chilensis (Hupe 1854) Sebastia. Aquaculture Research 38: 1770–1777.CrossRefGoogle Scholar
  32. Kurihara, H. 2008. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series 373: 275–284.CrossRefGoogle Scholar
  33. Langdon, C. and M.J. Atkinson. 2005. Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. Journal of Geophysical Research 110: C09S07.Google Scholar
  34. Langdon, C., T. Takahashi, C. Sweeney, D. Chipman, J. Goddard, F. Marubini, H. Aceves, H. Barnett, and M.J. Atkinson. 2000. Effect of calcium carbonate saturation state on the calcification rate of an experimental reef. Global Biogeochemical Cycles 14: 639–654.CrossRefGoogle Scholar
  35. Leclercq, N., J.P. Gattuso, and J. Jaubert. 2000. CO2 partial pressure controls the calcification rate of a coral community. Global Change Biology 6: 329–334.CrossRefGoogle Scholar
  36. Lewis, E., and D. Wallace. 1998. Program developed for CO 2 system calculations. Carbon Dioxide Information Analysis Center. Tennessee, U.S.A.: Oak Ridge.Google Scholar
  37. Manríquez, P.H., M.E. Jara, M.L. Mardones, J.M. Navarro, R. Torres, M.A. Lardies, C.A. Vargas, C. Duarte, S. Widdicombe, J. Salisbury, and N.A. Lagos. 2013. Ocean acidification disrupts prey responses to predator cues but not net prey shell growth in Concholepas concholepas (loco). PLoS ONE 8(7): e68643. doi: 10.1371/journal.pone.0068643.CrossRefGoogle Scholar
  38. Marshall, D.J., J.H. Santos, K.M.Y. Leung, and W.H. Chak. 2008. Correlations between gastropod shell dissolution and water chemical properties in a tropical estuary. Marine Environmental Research 66: 422–429.CrossRefGoogle Scholar
  39. Mehrbach, C., C.H. Culberson, J.E. Hawley, and R.N. Pytkowicz. 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18: 897–907.CrossRefGoogle Scholar
  40. Melzner, F., J. Thomsen, W. Koeve, A. Oschlies, M.A. Gutowska, H.W. Bange, H.P. Hansen, and A. Körtzinger. 2013. Future ocean acidification will be amplified by hypoxia in coastal habitats. Marine Biology 160: 1875–1888.CrossRefGoogle Scholar
  41. Michaelidis, B., C. Ouzounis, A. Paleras, and H.O. Pörtner. 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.CrossRefGoogle Scholar
  42. Miller, A.W., A.C. Reynolds, C. Sobrino, and G.F. Riedel. 2009. Shellfish face uncertain future in high CO2 world: influence of acidification on oyster larvae calcification and growth in estuaries. PLoS ONE 4(5): e5661. doi: 10.1371/journal.pone.0005661.CrossRefGoogle Scholar
  43. Navarro, J.M., R. Torres, K. Acuña, C. Duarte, P.H. Manríquez, M. Lardies, N.A. Lagos, C. Vargas, and V. Aguilera. 2013. Impact of medium-term exposure to elevated pCO2 levels on the physiological energetics of the mussel Mytilus chilensis. Chemosphere 90: 1242–1248.CrossRefGoogle Scholar
  44. Nienhuis, S., A.R. Palmer, and C.D.G. Harley. 2010. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proceeding of the Royal Society B: Biological Science 277: 2553–2558.CrossRefGoogle Scholar
  45. Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, R.M. Key, K. Lindsay, E. Maier-Reimer, R. Matear, P. Monfray, A. Mouchet, R.G. Najjar, G.-K. Plattner, K.B. Rodgers, C.L. Sabine, J.L. Sarmiento, R. Schlitzer, R.D. Slater, I.J. Totterdell, M.-F. Weirig, Y. Yamanaka, and A. Yool. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.CrossRefGoogle Scholar
  46. Palmer, A.R. 1982. Growth in marine gastropods: A non-destructive technique for independently measuring shell and body weight. Malacologia 23: 63–73.Google Scholar
  47. Pansch, C., A. Nasrolahi, Y.S. Appelhans, M. Wahl. 2013. Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2. Marine Biology 160: doi  10.1007/s00227-012-2069-4
  48. Parker, L.M., P.M. Ross, and W.A. O’Connor. 2011. Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Marine Biology. doi: 10.1007/s00227-010-1592-4.Google Scholar
  49. Parker, L.M., P.M. Ross, W.A. O’Connor, H.O. Pörtner, E. Scanes, and J.M. Wright. 2013. Predicting the response of molluscs to the impact of ocean acidification. Biology 2: 651–692.CrossRefGoogle Scholar
  50. Pascal, P.-Y., J.W. Fleeger, F. Galvez, and K.R. Carman. 2010. The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. Marine Pollution Bulletin 60: 2201–2208.CrossRefGoogle Scholar
  51. Range, P., M.A. Chícharo, R. Ben-Hamadou, D. Piló, D. Matias, S. Joaquim, A.P. Oliveira, and L. Chícharo. 2011. Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: Variable responses to ocean acidification at local scales? Journal of Experimental Marine Biology and Ecology 396: 177–184.CrossRefGoogle Scholar
  52. Range, P., M.A. Chicharo, R. Ben-Hamadou, D. Piló, and D. Matias. 2012. Effects of seawater acidification by CO2 on life history traits of juvenile mussels Mytilus galloprovincialis in a coastal lagoon environment. Journal of Experimental Marine Biology and Ecology 424–425: 89–98.CrossRefGoogle Scholar
  53. Range, P., M.A. Chícharo, R. Ben-Hamadou, D. Piló, M.J. Fernandez-Reiriz, U. Labarta and L. Chícharo. 2013. Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Regional Environmental Change: 1–12.Google Scholar
  54. Riebesell, U., I. Zondervan, B. Rost, P.D. Tortell, R.E. Zeebe, and F.M.M. Morel. 2000. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407: 364–367.CrossRefGoogle Scholar
  55. Ries, J.B., A.L. Cohen, and D.C. McCorkle. 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37(12): 1131–1134.CrossRefGoogle Scholar
  56. Sabine, C.L., R.A. Feely, N. Gruber, R.M. Key, K. Lee, J.L. Bullister, R. Wanninkhof, C.S. Wong, D.W.R. Wallace, B. Tilbrook, F.J. Millero, T.-H. Peng, A. Kozyr, T. Ono, and A.F. Rios. 2004. The ocean sink for anthropogenic CO2. Science 305: 367–371.CrossRefGoogle Scholar
  57. Salisbury, J., M. Green, C. Hunt, and J. Campbell. 2008. Coastal acidification by rivers: a new threat to shellfish? Eos, Transactions American Geophysical Union 89: 513.CrossRefGoogle Scholar
  58. Spicer, J.I., A. Raffo, and S. Widdicombe. 2007. Influence of CO2-related seawater acidification on extracellular acid–base balance in the velvet swimming crab Necora puber. Marine Biology 151: 1117–1125.CrossRefGoogle Scholar
  59. Sunday, J.M., R.N. Crim, C.D.G. Harley, and M.W. Hart. 2011. Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6(8): e22881. doi: 10.1371/journal.pone.0022881.CrossRefGoogle Scholar
  60. Talmage, S.C., and C.J. Gobler. 2009. The effects of elevated carbon dioxide concentrations on the metamorphosis, size and survival of larval hard clams (Mercenaria mercenaria), bay scallops (Argopecten irradians), and Eastern oysters (Crassostrea virginica). Limnology and Oceanography 54: 2072–2080.CrossRefGoogle Scholar
  61. Thomsen, J., and F. Melzner. 2010. Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Marine Biology 157: 2667–2676.CrossRefGoogle Scholar
  62. Thomsen, J., M.A. Gutowska, J. Saphörster, A. Heinemann, K. Trübenbach, J. Fietzke, C. Hiebenthal, A. Eisenhauer, A. Körtzinger, M. Wahl, and F. Melzner. 2010. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7: 3879–3891.CrossRefGoogle Scholar
  63. Thomsen, J., I. Casties, C. Pansch, A. Körtzinger, and F. Melzner. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Global Change Biology 19: 1017–1027.CrossRefGoogle Scholar
  64. Torres, R., P.H. Manriquez, C. Duarte, J.M. Navarro, N.A. Lagos, C.A. Vargas, and M.A. Lardies. 2013. Evaluation of a semi-automatic system for long-term seawater carbonate chemistry manipulation. Revista Chilena de Historia Natural 86: 443–451.CrossRefGoogle Scholar
  65. Tunnicliffe, V., K.T.A. Davies, D.A. Butterfield, R.W. Embley, J.M. Rose, and W.W. Chadwick Jr. 2009. Survival of mussels in extremely acidic waters on a submarine volcano. Nature Geoscience 2: 344–348.CrossRefGoogle Scholar
  66. Underwood, A.J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge: Cambridge University.Google Scholar
  67. Vargas, C.A., M. de la Hoz, V. Aguilera, V. San Martín, P.H. Manríquez, J.M. Navarro, R. Torres, M.A. Lardies, and N.A. Lagos. 2013. CO2-driven ocean acidification reduces larval feeding efficiency and change food selectivity in the mollusk Concholepas concholepas. Journal of Plankton Research. doi: 10.1093/plankt/fbt045.Google Scholar
  68. Vihtakari, M., I.E. Hendriks, J. Holding, P.E. Renaud, C.M. Duarte, and J.N. Havenhand. 2013. Effects of ocean acidification and warming on sperm activity and early life stages of the Mediterranean mussel (Mytilus galloprovincialis). Water 5: 1890–1915.CrossRefGoogle Scholar
  69. Widdicombe, S., and J.L. Spicer. 2008. Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? Journal of Experimental Marine Biology and Ecology 366: 187–197.CrossRefGoogle Scholar
  70. Widdicombe, S., S.L. Dashfield, C.L. McNeill, H.R. Needham, A. Beesley, A. McEvoy, S. Øxnevad, K.R. Clarke, and J.A. Berge. 2009. Impact of CO2 induced seawater acidification on sediment diversity and nutrient flux. Marine Ecology Progress Series 379: 59–75.CrossRefGoogle Scholar
  71. Wolf-Gladrow, D.A., U. Reibesell, S. Burkhardt, and J. Bijma. 1999. Direct effects of CO2 concentration on growth and isotopic composition of marine plankton. Tellus B 51: 461–476.CrossRefGoogle Scholar
  72. Wootton, J.T., C.A. Pfister and J.D. Forester. 2008. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. PLoS ONE 105 (48): doi  10.1073/pnas.0810079105.
  73. Zar, J.H. 1999. Biostatistical Analysis, 4th ed. Upper Saddle River: Prentice Hall.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2014

Authors and Affiliations

  • Cristian Duarte
    • 1
    • 2
  • Jorge M. Navarro
    • 3
  • Karin Acuña
    • 3
  • Rodrigo Torres
    • 4
  • Patricio H. Manríquez
    • 5
  • Marcos A. Lardies
    • 6
  • Cristian A. Vargas
    • 2
    • 7
  • Nelson A. Lagos
    • 8
  • Víctor Aguilera
    • 9
  1. 1.Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos NaturalesUniversidad Andres BelloSantiagoChile
  2. 2.Center for the Study of Multiple-drivers on Marine Socio-Ecological System (MUSELS)Universidad de ConcepciónConcepciónChile
  3. 3.Instituto de Ciencias Marinas y Limnológicas, Facultad de CienciasUniversidad Austral de ChileValdiviaChile
  4. 4.Centro de Investigación en Ecosistemas de la Patagonia (CIEP)CoyhaiqueChile
  5. 5.Laboratorio de Ecología y Conducta de la Ontogenia Temprana (LECOT)Centro de Estudios Avanzados en Zonas Áridas (CEAZA)CoquimboChile
  6. 6.Facultad de Artes LiberalesUniversidad Adolfo IbáñezSantiagoChile
  7. 7.Laboratorio de Funcionamiento de Ecosistemas Acuáticos (LAFE), Unidad de Sistemas Acuáticos, Centro de Ciencias Ambientales EULA ChileUniversidad de ConcepciónConcepciónChile
  8. 8.Centro de Investigación e Innovación para el Cambio Climático (CIICC), Facultad de CienciasUniversidad Santo TomasSantiagoChile
  9. 9.Instituto de Ciencias Naturales Alexander von HumboldtUniversidad de AntofagastaAntofagastaChile

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