Oceanography The Official Magazine of
The Oceanography Society
Volume 28 Issue 03

View Issue TOC
Volume 28, No. 3
Pages 36 - 45

OpenAccess

Assessing Ocean Acidification Variability in the Pacific-Arctic Region as Part of the Russian-American Long-term Census of the Arctic

By Nicholas R. Bates  
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

The Russian-American Long-term Census of the Arctic (RUSALCA) project provides a rare opportunity to study the Russian sector of the Pacific Arctic Region (PAR), which includes the Chukchi and East Siberian Seas. RUSALCA data from 2009 and 2012 allow fuller understanding of changes in ocean chemistry across this the region and, in particular, provide perspectives on the ocean carbon cycle, air-sea CO2 gas exchange, and ocean acidification variability. Summertime surface waters of the western Chukchi Sea and East Siberian Sea mostly exhibited low pCO2 (<100 to 400 µatm) and high pH (8.0 to 8.4) conditions during sea ice retreat. As earlier studies of the adjacent eastern Chukchi Sea show, this area of the PAR had a strong potential for ocean uptake of atmospheric CO2 , with saturation states for calcium carbonate (CaCO3) minerals such as calcite and aragonite (Ωcalcite and Ωaragonite, respectively) having values generally greater than two, thereby facilitating CaCO3 production. In contrast, fresher surface waters flowing into the Chukchi Sea from the East Siberian Sea and bottom waters on the PAR shelves exhibited high pCO2 and low pH, Ωcalcite, and Ωaragonite conditions. Low Ω surface waters near the Russian coast and nearly 70% of waters next to the seafloor were corrosive to CaCO3 minerals such as aragonite, with this change seemingly occurring at a more rapid rate than typical global open-ocean changes in ocean chemistry. The exposure of subsurface benthic communities and nearshore ecosystems near the Russian coast to potentially corrosive water is likely exacerbated by the ocean uptake of anthropogenic CO2 and gradual ocean acidification. The RUSALCA project also highlights the complexities and uncertainties in the physical and biogeochemical drivers of the ocean carbon cycle and ocean chemistry in this region of the Arctic.

Citation

Bates, N.R. 2015. Assessing ocean acidification variability in the Pacific-Arctic region as part of the Russian-American Long-term Census of the Arctic. Oceanography 28(3):36–45, https://doi.org/​10.5670/oceanog.2015.56.

References
    Anderson, L.G., S. Jutterstrom, S. Hjalmarsson, I. Wahlström, and I.P. Semiletov. 2009. Out-gassing of CO2 from Siberian Shelf seas by terrestrial organic matter decomposition. Geophysical Research Letters 36, L20601,https://doi.org/10.1029/2009GL040046.
  1. Anderson, L.G., G. Björk, S. Jutterström, I. Pipko, N. Shakhova, I. Semiletov, and I. Wåhlström. 2011. East Siberian Sea, an Arctic region of very high biogeochemical activity. Biogeosciences 8:1,745–1,754, https://doi.org/10.5194/bg-8-1745-2011.
  2. Ardyna, M., M. Babin, M. Gosselin, E. Devrad, L. Rainville, and J.-E. Tremblay. 2014. Recent Arctic Ocean sea-ice loss triggers novel fall phytoplankton blooms. Geophysical Research Letters 41:6,207–6,212,https://doi.org/10.1002/2014GL061047.
  3. Arrigo, K.R., and G. van Dijken. 2011. Secular trends in Arctic Ocean net primary production. Journal of Geophysical Research 116, C09011, https://doi.org/10.1029/2011JC007151.
  4. Arrigo, K.R., G. van Dijken, and S. Pabi. 2008. Impact of a shrinking Arctic ice cover on marine primary production.Geophysical Research Letters 35, L19603, https://doi.org/10.1029/2008GL035028.
  5. Arrigo, K.J., D.K. Perovich, R.S. Pickart, Z.W. Brown, G.L. van Dijken, K.E. Lowry, M.M. Mills, M.A. Palmer, W.M. Balch, N.R. Bates, and others. 2012. Massive phytoplankton blooms under Arctic sea-ice. Science 336:1,408–1,409,https://doi.org/10.1126/science.1215065.
  6. Arrigo, K.R., D.K. Perovich, R.S. Pickart, Z.W. Brown, G.L. van Dijken, K.E. Lowry, M.M. Mills, M.A. Palmer, W.B. Balch, N.R. Bates, and others. 2014. Phytoplankton blooms beneath the sea ice in the Chukchi Sea. Deep-Sea Research 105:1–16, https://doi.org/10.1016/j.dsr2.2014.03.018.
  7. Bates, N.R. 2006. Air-sea CO2 fluxes and the continental shelf pump of carbon in the Chukchi Sea adjacent to the Arctic Ocean. Journal of Geophysical Research 111, C10013, https://doi.org/10.1029/2005JC003083.
  8. Bates, N.R. 2007. Interannual variability of the oceanic carbon dioxide sink in the subtropical gyre of the North Atlantic Ocean over the last two decades. Journal of Geophysical Research 112, C09013,https://doi.org/10.1029/2006JC003759.
  9. Bates, N.R., and J.T. Mathis. 2009. The Arctic Ocean marine carbon cycle: Evaluation of air-sea CO2 exchanges, ocean acidification impacts and potential feedbacks. Biogeosciences 6:2,433–2,459, https://doi.org/10.5194/bg-6-2433-2009.
  10. Bates, N.R., M.H.P. Best, and D.A. Hansell. 2005. Spatio-temporal distribution of dissolved inorganic carbon and net community production in the Chukchi and Beaufort Seas. Deep Sea Research II 52:3,303–3,323,https://doi.org/10.1016/j.dsr2.2005.10.005.
  11. Bates, N.R., S.B. Moran, D.A. Hansell, and J.T. Mathis. 2006. An increasing CO2 sink in the Arctic Ocean due to sea-ice loss? Geophysical Research Letters 33, L23609, https://doi.org/10.1029/2006GL027028.
  12. Bates, N.R., J.T. Mathis, and L. Cooper. 2009. Ocean acidification and biologically induced seasonality of carbonate mineral saturation states in the western Arctic Ocean. Journal of Geophysical Research 114, C11007,https://doi.org/10.1029/2008JC004862.
  13. Bates, N.R., M.H. Best, K. Neely, R. Garley, A.G. Dickson, and R.J. Johnson. 2012. Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean. Biogeosciences 9:2,509–2,522, https://doi.org/10.5194/bg-9-2509-2012.
  14. Bates, N.R., M.A. Jeffries, and J.T. Mathis. 2011. Air-sea CO2 fluxes in the Bering Sea. Biogeosciences 8(5):1,237–1,253,https://doi.org/10.5194/bg-8-1237-2011.
  15. Bates, N.R., M.I. Orchowska, R. Garley, and J.T. Mathis. 2013. Summertime calcium carbonate undersaturation in shelf waters of the western Arctic Ocean: How biological processes exacerbate the impact of ocean acidification. Biogeosciences10:5,281–5,309, https://doi.org/10.5194/bg-10-5281-2013.
  16. Bates, N.R., Y.M. Astor, M.J. Church, K. Currie, J.E. Dore, M. Gonzalez-Davila, L. Lorenzoni, F.E. Muller Karger, J. Olafsson, and J.M. Santana-Casiano. 2014a. A time-series view of changing ocean chemistry due to ocean uptake of anthropogenic CO2 and ocean acidification. Oceanography 27(1):126–141, https://doi.org/10.5670/oceanog.2014.16.
  17. Bates, N.R., R. Garley, K. Frey, K. Shake, and J.T. Mathis. 2014b. Sea-ice melt CO2-carbonate chemistry in the western Arctic: Meltwater contributions to air-sea CO2 gas exchange, mixed layer properties and rates of net community production.Biogeosciences 11:6,769–6,789, https://doi.org/10.5194/bg-11-6769-2014.
  18. Brewer, P.G., and J.C. Goldman. 1976. Alkalinity changes generated by phytoplankton growth. Limnology and Oceanography 21:108–117, https://doi.org/10.4319/lo.1976.21.1.0108.
  19. Butler, J.N. 1991. Carbon Dioxide Equilibria and Their Applications. Addison-Wesley Publications, 272 pp.
  20. Cai, W.J., N.R. Bates, L. Guo, L.G. Anderson, J.T. Mathis, R. Wanninkhof, D.A. Hansell, L. Chen, and I. Semiletov. 2014. Carbon fluxes across boundaries in the Pacific Arctic region in a changing environment. Pp. 199–222 in The Pacific Arctic Sector: Status and Trends. J.M. Grebmeier, W. Maslowski, and J. Zhao, eds, Springer.
  21. Caldeira, K., and M.E. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425:365–368,https://doi.org/10.1038/425365a.
  22. Caldeira, K., and M.E. Wickett. 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research 110, C09S04, https://doi.org/10.1029/2004JC002671.
  23. Carmack, E., and P. Wassmann. 2006. Food webs and physical-biological coupling on pan-Arctic shelves: Unifying concepts and comprehensive perspectives. Progress in Oceanography 71:446–477,https://doi.org/10.1016/j.pocean.2006.10.004.
  24. Codispoti, L.A., V. Kelly, A. Thessen, P. Matrai, S. Suttles, V. Hill, M. Steele, and B. Light. 2013. Synthesis of primary production in the Arctic Ocean: Part III. Nitrate and phosphate based estimates of net community production. Progress in Oceanography 110:126–150, https://doi.org/10.1016/j.pocean.2012.11.006.
  25. Cross, J.N., J.T. Mathis, and N.R. Bates. 2013. Conservative and non-conservative variations of total alkalinity on the southeastern Bering Sea. Marine Chemistry 154:100–112, https://doi.org/10.1016/j.marchem.2013.05.012.
  26. Cross, J.N., J.T. Mathis, K.E. Frey, C.E. Cosca, S.L. Danielson, N.R. Bates, T. Takahashi, and W. Evans. 2014. Annual sea-air CO2 fluxes in the Bering Sea: Insights from new autumn and winter observations of a seasonally ice-covered continental shelf. Journal of Geophysical Research 119:6,693–6,708, https://doi.org/10.1002/2013JC009579.
  27. 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 Part A 34:1,733–1,743, https://doi.org/10.1016/0198-0149(87)90021-5.

  28. Dickson, A.G., C.L. Sabine, and J.R. Christian. 2007. Guide to Best Practices for Ocean CO2 Measurements. PICES Special Publication 3, IOCCP Report no. 8, 191 pp.
  29. 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 1:169–192, https://doi.org/10.1146/annurev.marine.010908.163834.
  30. Evans, W.R., J.T. Mathis, J.N. Cross, N.R. Bates, K.E. Frey, B.T. Else, T.N. Papyriakou, M. DeGrandpre, F. Islam, W.-J. Cai, and others. 2015. Sea-air CO2 exchange in the western Arctic coastal ocean. Global Biogeochemical Cycles 29,https://doi.org/10.1002/2015GB005153.
  31. Feely, R.A., S.C. Doney, and S.R. Cooley. 2009. Ocean acidification: Present and future changes in a high-CO2 world.Oceanography 22(4):36–47, https://doi.org/10.5670/oceanog.2009.95.
  32. Frey, K.E., J.A. Maslanik, J.C. Kinney, and W. Maslowski. 2014. Recent variability in sea-ice cover, age, and thickness in the Pacific Arctic Region. Pp. 31–63 in The Pacific Arctic Sector: Status and Trends. J.M. Grebmeier, W. Maslowski, and J. Zhao, eds, Springer.
  33. Grebmeier, J.M., N.R. Bates, and A. Devol. 2008. Continental margins of the Arctic Ocean and Bering Sea. Pp. 61–72 in North American Continental Margins: A Synthesis and Planning Workshop. B. Hales, W.-J. Cai., B.G. Mitchell, C.L. Sabine, and O. Schofield, eds, US Carbon Cycle Science Program, Washington, DC.
  34. Grebmeier, J.M., S.E. Moore, J.E. Overland, K.E. Frey, and R. Gradinger. 2010. Biological response to recent Pacific Arctic sea-ice retreats. Eos Transactions, American Geophysical Union 91:161–162, https://doi.org/10.1029/2010EO180001.
  35. Hill, V.J., and G.F. Cota. 2005. Spatial patterns of primary production in the Chukchi Sea in the spring and summer of 2002.Deep Sea Research Part II 52:3,344–3,354, https://doi.org/10.1016/j.dsr2.2005.10.001.
  36. Kahru, M., R.M. Kudela, R. Murtugudde, P.G. Strutton, M. Manzano-Sarabia, H. Wang, and B.G. Mitchell. 2010. Global correlations between winds and ocean chlorophyll. Journal of Geophysical Research 115, C12040,https://doi.org/10.1029/2010JC006500.
  37. Lalande, C., S. Belanger, and L. Fortier. 2009. Impact of a decreasing sea ice cover on the vertical export of particulate organic carbon in the northern Laptev sea, Siberian Arctic Ocean. Geophysical Research Letters 36, L21604,https://doi.org/10.1029/2009GL040570.
  38. Lalande, C., E.M. Nöthig, E. Bauerfeind, and L. Fortier. 2014. Export fluxes of biogenic matter in the Siberian Arctic Ocean. Paper presented at the Ocean Sciences Meeting, Honolulu, Hawaii.
  39. Lewis, S.L., and M.A. Maslin. 2015. Defining the Anthropocene. Nature 519:171–180,https://doi.org/10.1038/nature14258.
  40. Li, W.K.W., F.A. McLaughlin, C. Lovejoy, and E.C. Carmack. 2009. Smallest algae thrive as the Arctic Ocean freshens.Science 326:539, https://doi.org/10.1126/science.1179798.
  41. Lowry, K.E., R.S. Pickart, M.M. Mills, Z.W. Brown, G.L. van Dijken, N.R. Bates, and K.R. Arrigo. 2015. The influence of winter water on phytoplankton blooms in the Chukchi Sea. Deep Sea Research Part II 118:53–57,https://doi.org/10.1016/j.dsr2.2015.06.006.
  42. MacGilchrist, G.A., A.C. Naveira Garabato, T. Tsubouchi, S. Bacon, S. Torres-Valdes, and K. Aezetsu-Scott. 2014. The Arctic Ocean carbon sink. Deep-Sea Research Part I 86:39–55, https://doi.org/10.1016/j.dsr.2014.01.002.
  43. Manizza, M., M.J. Follows, S. Dutkiewicz, D. Menemenlis, C.N. Hill, and R.M. Key. 2013. Changes in the Arctic Ocean CO2sink (1996–2007): A regional model analysis. Global Biogeochemical Cycles 27:1,108–1,118,https://doi.org/10.1002/2012GB004491.
  44. Markus, T., J. Stroeve, and J. Miller. 2009. Recent changes in Arctic sea ice melt onset, freeze up and melt season length.Journal of Geophysical Research 114, C12024, https://doi.org/10.1029/2009JC005436.
  45. Mathis, J.T., N.R. Bates, D.A. Hansell, and T. Babila. 2009. Net community production in the northeastern Chukchi Sea. Deep Sea Research Part II 56:1,213–1,222, https://doi.org/10.1016/j.dsr2.2008.10.017.
  46. Mathis, J.T., J. Cross, and N.R. Bates. 2011a. Coupling primary production and terrestrial runoff to ocean acidification and carbonate mineral suppression in the eastern Bering Sea. Global Biogeochemical Cycles 116, C02030,https://doi.org/10.1029/2010JC006453.
  47. Mathis, J.T., J. Cross, and N.R. Bates. 2011b. The role of ocean acidification in systemic carbonate mineral suppression in the Bering Sea. Geophysical Research Letters 38, L19602, https://doi.org/10.1029/2011GL048884.
  48. Mathis, J.T., J.M. Grebmeier, D.A. Hansell, R.R. Hopcroft, D.L. Kirchman, S.H. Lee, S.B. Moran, and N.R. Bates. 2014. Carbon biogeochemistry of the western Arctic: Production, export, and ocean acidification. Pp. 223–268 in The Pacific Arctic Sector: Status and Trends. J.M. Grebmeier, W. Maslowski, and J. Zhao, eds, Springer.
  49. Mehrbach, C., C.H. Culberson, J.E. Hawley, and R.M. Pytkowicz. 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18:897–907,https://doi.org/10.4319/lo.1973.18.6.0897.
  50. Murata, A., and T. Takizawa. 2003. Summertime CO2 sinks in shelf and slope waters of the western Arctic Ocean.Continental Shelf Research 23:753–776, https://doi.org/10.1016/S0278-4343(03)00046-3.
  51. Nishino, S., T. Kikichi, M. Yamamoto-Kawai, Y. Kawaguchi, T. Hirawake, and M. Itoh. 2011. Enhancement/reduction of biological pump depends on ocean circulation in the sea-ice reduction regions of the Arctic Ocean. Journal of Oceanography 67:305–311, https://doi.org/10.1007/s10872-011-0030-7.
  52. Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, and others. 2005. Anthropogenic ocean acidification over the twenty-first century and its impacts on calcifying organisms. Nature 437:681–686, https://doi.org/10.1038/nature04095.
  53. Overland, J.E, and M. Wang. 2013. When will the summer Arctic be nearly sea-ice free? Geophysical Research Letters 40:2,097–2,101, https://doi.org/10.1002/grl.50316.
  54. Perovich, D.K., and J.A. Richter-Menge. 2009. Loss of sea ice in the Arctic. Annual Review of Marine Science 1:417–441,https://doi.org/10.1146/annurev.marine.010908.163805.
  55. Perovich, D.K., B. Light, H. Eicken, K.F. Jones, K. Runciman, and S.V. Nghiem. 2007. Increasing solar heating of the Arctic Ocean and adjacent seas, 1979–2005: Attribution and role in the ice-albedo feedback. Geophysical Research Letters 34, L19505, https://doi.org/10.1029/2007GL031480.
  56. Pipko, I.I., I.P. Semiletov, P.A. Tischenko, S.P. Pugach, and J.P. Christensen. 2002. Carbonate chemistry dynamics in Bering Strait and Chukchi Sea. Progress in Oceanography 55:77–94, https://doi.org/10.1016/S0079-6611(02)00071-X.
  57. Rhein, M., S.R. Rintoul, S. Aoki, E. Campos, D. Chambers, R.A. Feely, S. Gulev, G.C. Johnson, S.A. Josey, A. Kostianoy, and others. 2013. Observations: Ocean. Chapter 3 in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T.F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P.M. Midgley, eds, Cambridge University Press, Cambridge, UK, and New York, NY, USA.
  58. Robbins, L.L., M.E. Hansen, J.A. Kleypas, and S.C. Meylan. 2010. CO2calc: A User-Friendly Seawater Carbon Calculator for Windows, Max OS X, and iOS (iPhone). US Geological Survey Open-File Report, 2010–1280, 17 pp.,http://pubs.usgs.gov/of/2010/1280.
  59. Schlitzer, R., 2011. Ocean Data Viewhttp://odv.awi.de.
  60. Schuster, U., G. McKinley, N.R. Bates, F. Chevallier, S.C. Doney, A. Fay, M. Gonzaléz-Dávila, N. Gruber, S. Jones, P. Landschützer, and others. 2013. An assessment of the Atlantic and Arctic sea–air CO2 fluxes, 1990–2009. Biogeosciences 10:607–627, https://doi.org/10.5194/bg-10-607-2013.
  61. Screen, J.A., C. Deser, I. Simmonds, and R. Tomas. 2013. Atmospheric impacts of Arctic sea-ice loss, 1979–2009: Separating forced change from atmospheric internal variability. Climate Dynamics 43:333–344,https://doi.org/10.1007/s00382-013-1830-9.
  62. Semiletov, I.P., A. Makshtas, S.I. Akasofu, and E.L. Andreas. 2004. Atmospheric CO2 balance: The role of Arctic sea ice.Geophysical Research Letters 31, L05121, https://doi.org/10.1029/2003GL017996.
  63. Semiletov, I., I. Pipko, I. Repina, and N.E. Shakhova. 2007. Carbonate chemistry dynamics and carbon dioxide fluxes across the atmosphere-ice-water interfaces in the Arctic Ocean: Pacific sector of the Arctic. Journal of Marine Systems 66:204–226, https://doi.org/10.1016/j.jmarsys.2006.05.012.
  64. Simmonds, I., and P.D. Govekar. 2014. What are the physical links between Arctic sea-ice loss and Eurasian winter climate? Environmental Research Letters 9, 101003, https://doi.org/10.1088/1748-9326/9/10/101003.
  65. Steinacher, M., F. Joos, T.L. Frölicher, G.-K. Plattner, and S.C. Doney. 2009. Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6:515–533,https://doi.org/10.5194/bg-6-515-2009.
  66. Stroeve, J.C., M.M. Holland, W. Meier, T. Scambos, and M. Serreze. 2007. Arctic sea ice decline: Faster than forecast.Geophysical Research Letters 34, L09501, https://doi.org/10.1029/2007GL029703.
  67. Stroeve, J.C., T. Markus, L. Boisvert, J. Miller, and A. Barrett. 2014. Changes in Arctic melt season and implications for sea-ice loss. Geophysical Research Letters 41:1,216–1,225, https://doi.org/10.1002/2013GL058951.
  68. Stumm, W., and Morgan, J.J., 1981. Aquatic Chemistry: An Introduction Emphasizing Chemical Equilibria in Natural Waters. John Wiley and Sons, New York, 780 pp.
  69. Takahashi, T., S.C. Sutherland, C. Sweeney, A. Poisson, N. Metzl, B. Tilbrook, N.R. Bates, R. Wanninkhof, R.A. Feely, C. Sabine, and others. 2002. Global sea-air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects. Deep Sea Research Part II 49:1,601–1,622, https://doi.org/10.1016/S0967-0645(02)00003-6.
  70. Takahashi, T., S.C. Sutherland, R. Wanninkhof, C. Sweeney, R.A. Feely, D.W. Chipman, B. Hales, G. Friederich, F. Chavez, A. Watson, and others. 2009. Climatological mean and decadal change in surface ocean pCO2, and net sea-air CO2 flux over the global oceans. Deep Sea Research Part II 56:554–577, https://doi.org/10.1016/j.dsr2.2008.12.009.
  71. Wang, M., and J.E. Overland. 2009. A sea ice free summer Arctic within 30 years? Geophysical Research Letters 36, L07502, https://doi.org/10.1029/2009GL037820.
  72. Wassmann, P., C.M. Duarte, S. Agusti, and M.K. Sejr. 2011. Footprints of climate change in the Arctic marine ecosystem.Global Change Biology 17:1,235–1,249, https://doi.org/10.1111/j.1365-2486.2010.02311.x.
  73. Weingartner, T.J., S. Danielson, Y. Sasaki, V. Pavlov, and M. Kulakov. 1999. The Siberian Coastal Current: A wind- and buoyancy-forced Arctic coastal current. Journal of Geophysical Research 104:29,697–29,713,https://doi.org/10.1029/1999JC900161.
  74. Zeebe, R.E., and D. Wolf-Gladrow. 2001. CO2 in Seawater: Equilibrium, Kinetics, Isotopes. Elsevier, Amsterdam.
Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.