Oceanography The Official Magazine of
The Oceanography Society
Volume 27 Issue 01

View Issue TOC
Volume 27, No. 1
Pages 222 - 235


Sixty Years of Sverdrup: A Retrospective of Progress in the Study of Phytoplankton Blooms

By Alexis D. Fischer , Emily A. Moberg , Harriet Alexander, Emily F. Brownlee, Kristen R. Hunter-Cevera, Kathleen J. Pitz, Sarah Z. Rosengard, and Heidi M. Sosik  
Jump to
Article Abstract Citation Supplementary Materials References Copyright & Usage
Article Abstract

One of the most dramatic large-scale features in the ocean is the seasonal greening of the North Atlantic in spring and summer due to the accumulation of phytoplankton biomass in the surface layer. In 1953, Harald Ulrik Sverdrup hypothesized a now canonical mechanism for the development and timing of phytoplankton blooms in the North Atlantic. Over the next 60 years, Sverdrup’s Critical Depth Hypothesis spurred progress in understanding of bloom dynamics and offered a valuable theoretical framework on which to build. In reviewing 60 years of literature, the authors trace the development of modern bloom initiation hypotheses, highlighting three case studies that illuminate the complexity, including both catalysts and impediments, of scientific progress in the wake of Sverdrup’s hypothesis. Most notably, these cases demonstrate that the evolution of our understanding of phytoplankton blooms was paced by access not only to technology but also to concurrent insights from several disciplines. This exploration of the trajectories and successes in bloom studies highlights the need for expanding interdisciplinary collaborations to address the complexity of phytoplankton bloom dynamics.


Fischer, A.D., E.A. Moberg, H. Alexander, E.F. Brownlee, K.R. Hunter-Cevera, K.J. Pitz, S.Z. Rosengard, and H.M. Sosik. 2014. Sixty years of Sverdrup: A retrospective of progress in the study of phytoplankton blooms. Oceanography 27(1):222–235, https://doi.org/10.5670/oceanog.2014.26.

Supplementary Materials

Anderson, G.C. 1964. The seasonal and geographic distribution of primary productivity off the Washington and Oregon coasts. Limnology and Oceanography 9:284–302, https://doi.org/10.4319/lo.1964.9.3.0284.

Apollonio, S. 1980. Primary production in Dumbell Bay in the Arctic Ocean. Marine Biology 61:41–51, https://doi.org/10.1007/BF00410340.

Aron, W. 1959. Midwater trawling studies in the North Pacific. Limnology and Oceanography 4:409–418, https://doi.org/10.4319/lo.1959.4.4.0409.

Azam, F., T. Fenchel, and J. Field. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10:257–263, https://doi.org/10.3354/meps010257.

Backhaus, J., H. Wehde, E. Hegseth, and J. Kämpf. 1999. “Phyto-convection”: The role of oceanic convection in primary production. Marine Ecology Progress Series 189:77–92, https://doi.org/10.3354/meps189077.

Banse, K. 1992. Grazing, temporal changes of phytoplankton concentrations, and the microbial loop in the open sea. Pp. 409–440 in Primary Productivity and Biogeochemical Cycles in the Sea. P.G. Falkowski and A.D. Woodhead eds., Plenum Press, NY, New York, USA.

Banse, K. 2002. Steemann Nielsen and the zooplankton. Hydrobiologia 480:15–28, https://doi.org/10.1023/A:1021220714899.

Behrenfeld, M.J. 2010. Abandoning Sverdrup’s critical depth hypothesis on phytoplankton blooms. Ecology 91:977–989, https://doi.org/10.1890/09-1207.1.

Behrenfeld, M.J., and E.S. Boss. 2013. Resurrecting the ecological underpinnings of ocean plankton blooms. Annual Review of Marine Science 6:1–28, https://doi.org/10.1146/annurev-marine-052913-021325.

Bigelow, H.B. 1926. Plankton of the Offshore Waters of the Gulf of Maine. Bulletin of the US Bureau of Fisheries, No. 40, Document 968, 509 pp. (quote from p. 465).

Boccaletti, G., R. Ferrari, and B. Fox-Kemper. 2007. Mixed layer instabilities and restratification. Journal of Physical Oceanography 37:2,228–2,250, https://doi.org/10.1175/JPO3101.1.

Breitbart, M. 2012. Marine viruses: Truth or dare. Annual Review of Marine Science 4:425–448, https://doi.org/10.1146/annurev-marine-120709-142805.

Briggs, N., M.J. Perry, I. Cetinić, C. Lee, E. D’Asaro, A.M. Gray, and E. Rehm. 2011. High-resolution observations of aggregate flux during a sub-polar North Atlantic spring bloom. Deep Sea Research Part I 58:1,031–1,039, https://doi.org/10.1016/j.dsr.2011.07.007.

Browne, C. 1942. Liebig and the law of the minimum. Pp. 71–82 in Liebig and after Liebig: A Century of Progress in Agricultural Chemistry. F.R. Moulton, ed., American Association for the Advancement of Science, Washington, DC.

Chisholm, S.W., S.L. Frankel, R. Goericke, R.J. Olson, B. Palenik, J.B. Waterbury, L. West-Johnsrud, and E.R. Zettler. 1992. Prochlorococcus marinus nov. gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Archives of Microbiology 157:297–300, https://doi.org/10.1007/BF00245165.

Chisholm, S.W., R.J. Olson, E.R. Zettler, R. Goericke, J.B. Waterbury, and N.A. Welschmeyer. 1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334:340–343, https://doi.org/10.1038/334340a0.

Claustre, H., Y. Huot, I. Obernosterer, B. Gentili, D. Tailliez, and M. Lewis. 2008. Gross community production and metabolic balance in the South Pacific Gyre, using a non intrusive bio-optical method. Biogeosciences 5:463–474.

Conover, S.A.M. 1975. Nitrogen utilization during spring blooms of marine phytoplankton in Bedford Basin, Nova Scotia, Canada. Marine Biology 32:247–261, https://doi.org/10.1007/BF00399204.

Coste, B., J. Gostan, and H.J. Minas. 1972. Influence of winter conditions on phytoplankton and zooplankton production in northwestern part of Mediterranean: Part 1. Hydrological structures and nutrient distribution. Marine Biology 16:320–348.

Cushing, D.H. 1959. The seasonal variation in oceanic production as a problem in population dynamics. Journal du Conseil International pour l’Exploration de la Mer 24:455–464, https://doi.org/10.1093/icesjms/24.3.455.

Dale, T., F. Rey, and B. Heimdal. 1999. Seasonal development of phytoplankton at a high latitude oceanic site. Sarsia 85:419–435.

Davis, C.S., S.M. Gallager, M. Marra, and W.K. Stewart. 1996. Rapid visualization of plankton abundance and taxonomic composition using the Video Plankton Recorder. Deep Sea Research Part II 43:1,947–1,970, https://doi.org/10.1016/S0967-0645(96)00051-3.

Denman, K., and A. Gargett. 1983. Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean. Limnology and Oceanography 28:801–815, https://doi.org/10.4319/lo.1983.28.5.0801.

Dillon, T.M., and D.R. Caldwell. 1980. The Batchelor spectrum and dissipation in the upper ocean. Journal of Geophysical Research 85:1,910–1,916, https://doi.org/10.1029/JC085iC04p01910.

Droop, M.R. 1974. Nutrient status of algal cells in continuous culture. Journal of the Marine Biological Association of the United Kingdom 54:825–855.

Ebert, U., M. Arrayás, N. Temme, B. Sommeijer, and J. Huisman. 2001. Critical conditions for phytoplankton blooms. Bulletin of Mathematical Biology 63:1,095–1,124, https://doi.org/10.1006/bulm.2001.0261.

Eilertsen, H.C. 1993. Spring blooms and stratification. Nature 363:24, https://doi.org/10.1038/363024a0.

Eilertsen, H., S. Sandberg, and H. Tøllefsen. 1995. Photoperiodic control of diatom spore growth: A theory to explain the onset of phytoplankton blooms. Marine Ecology Progress Series 116:303–307.

Evans, G., and J. Parslow. 1985. A model of annual plankton cycles. Biological Oceanography 3:327–347.

Fenchel, T. 1982. Ecology of heterotrophic microflagellates: Part II. Bioenergetics and growth. Marine Ecology Progress Series 8:225–231.

Fitzwater, S., G. Knauer, and J. Martin. 1982. Metal contamination and its effect on primary production measurements. Limnology and Oceanography 27:544–551.

Fogg, G.E. 1991. The phytoplanktonic ways of life. New Phytologist 118:191–232, https://doi.org/10.1111/j.1469-8137.1991.tb00974.x.

Fox-Kemper, B., R. Ferrari, and R. Hallberg. 2008. Parameterization of mixed layer eddies. Part I: Theory and diagnosis. Journal of Physical Oceanography 38:1,145–1,165, https://doi.org/10.1175/2007JPO3792.1.

Francisco, D., R. Mah, and A. Rabin. 1973. Acridine orange-epifluorescence technique for counting bacteria in natural waters. Journal of the American Microscopical Society 92:416–421.

Franks, P.J.S. 2002. NPZ models of plankton dynamics: Their construction, coupling to physics, and application. Journal of Oceanography 58:379–387, https://doi.org/10.1023/A:1015874028196.

Gallegos, C.L., and T. Platt. 1982. Phytoplankton production and water motion in surface mixed layers. Deep Sea Research Part A 29:65–76, https://doi.org/10.1016/0198-0149(82)90061-9.

Ghosal, S., and S. Mandre. 2003. A simple model illustrating the role of turbulence on phytoplankton blooms. Journal of Mathematical Biology 46:333–346, https://doi.org/10.1007/s00285-002-0184-4.

Gran, H., and T. Braarud. 1935. A quantitative study on the phytoplankton of the Bay of Fundy and the Gulf of Maine (including observations on hydrography, chemistry and morbidity). Journal of the Biological Board of Canada 1:219–467.

Grant, H.L., B. Hughes, W. Vogel, and A. Moilliet. 1968a. The spectrum of temperature fluctuations in turbulent flow. Journal of Fluid Mechanics 34:423–442, https://doi.org/10.1017/S0022112068001990.

Grant, H.L., A. Moilliet, and W.M. Vogel. 1968b. Some observations of the occurrence of turbulence in and above the thermocline. Journal of Fluid Mechanics 34:443–448, https://doi.org/10.1017/S0022112068002004.

Grant, H.L., R. Stewart, and A. Moilliet. 1962. Turbulence spectra from a tidal channel. Journal of Fluid Mechanics 12:241–268, https://doi.org/10.1017/S002211206200018X.

Gregg, M. 1991. The study of mixing in the ocean: A brief history. Oceanography 4(1):39–45, https://doi.org/10.5670/oceanog.1991.21.

Hansen, G., and H. Eilertsen. 1995. Modelling the onset of phytoplankton blooms: A new approach. Pp. 73–83 in Ecology of Fjords and Coastal Waters. Elsevier Sciences BV, Amsterdam.

Heimdal, B. 1974. Composition and abundance of phytoplankton in the Ullsfjord area, North Norway. Astarte 7:17–42.

Hobbie, J., R. Daley, and S. Jasper. 1977. Use of nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33:1,225–1,228.

Hollibaugh, J., D.L.R. Seibert, and W.H. Thomas. 1981. Observations on the survival and germination of resting spores of three Chaetoceros (Bacillariophyceae) species. Journal of Phycology 17:1–9, https://doi.org/10.1111/j.1529-8817.1981.tb00812.x.

Huisman, J., M. Arrayás, U. Ebert, and B. Sommeijer. 2002. How do sinking phytoplankton species manage to persist? The American Naturalist 159:245–254, https://doi.org/10.1086/338511.

Huisman, J., P. van Oostveen, and F.J. Weissing. 1999. Critical depth and critical turbulence: Two different mechanisms for the development of phytoplankton blooms. Limnology and Oceanography 44:1,781–1,787.

Huntsman, S.A., and W.G. Sunda. 1980. The role of trace metals in regulating phytoplankton growth with emphasis on Fe, Mn and Cu [iron, manganese, copper]. Studies in Ecology 7.

Kierstead, H., and L. Slobodkin. 1953. The size of water masses containing plankton blooms. Journal of Marine Research 12:141–147.

Körtzinger, A., U. Send, R.S. Lampitt, S. Hartman, D.W.R. Wallace, J. Karstensen, M.G. Villagarcia, O. Llinás, and M.D. DeGrandpre. 2008. The seasonal pCO2 cycle at 49°N/16.5°W in the northeastern Atlantic Ocean and what it tells us about biological productivity. Journal of Geophysical Research 113, C04020, https://doi.org/10.1029/2007JC004347.

Landry, M., R. Barber, R. Bidigare, F. Chai, K. Coale, H. Dam, M. Lewis, S. Lindley, J. McCarthy, M. Roman, and others. 1997. Iron and grazing constraints on primary production in the central equatorial Pacific: An EqPac synthesis. Limnology and Oceanography 42:405–418, https://doi.org/10.4319/lo.1997.42.3.0405.

Landry, M., and R. Hassett. 1982. Estimating the grazing impact of marine micro-zooplankton. Marine Biology 67:283–288, https://doi.org/10.1007/BF00397668.

Landry, M., J. Kirshtein, and J. Constantinou. 1995. A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific. Marine Ecology Progress Series 120:53–63, https://doi.org/10.3354/meps120053.

Lewis, M.R., D. Hebert, W.G. Harrison, T. Platt, and N.S. Oakey. 1986. Vertical nitrate fluxes in the oligotrophic ocean. Science 234:870–873, https://doi.org/10.1126/science.234.4778.870.

Mahadevan, A., E. D’Asaro, C. Lee, and M.J. Perry. 2012. Eddy-driven stratification initiates North Atlantic spring phytoplankton blooms. Science 337:54–58, https://doi.org/10.1126/science.1218740.

Mahadevan, A., and A. Tandon. 2006. An analysis of mechanisms for submesoscale vertical motion at ocean fronts. Ocean Modelling 14:241–256, https://doi.org/10.1016/j.ocemod.2006.05.006.

Marra, J. 1978a. Effect of short-term variations in light intensity on photosynthesis of a marine phytoplankter: A laboratory simulation study. Marine Biology 46:191–202, https://doi.org/10.1007/BF00390680.

Marra, J. 1978b. Phytoplankton photosynthetic response to vertical movement in a mixed layer. Marine Biology 46:203–208, https://doi.org/10.1007/BF00390681.

Marra, J., and R. Barber. 2005. Primary productivity in the Arabian Sea: A synthesis of JGOFS data. Progress in Oceanography 65:159–175, https://doi.org/10.1016/j.pocean.2005.03.004.

Martin, J.H., R.M. Gordon, and S.E. Fitzwater. 1990. Iron in Antarctic waters. Nature 345:156–158, https://doi.org/10.1038/345156a0.

Menzel, D.W., and J.H. Ryther. 1961. Annual variations in primary production of the Sargasso sea off Bermuda. Deep Sea Research 7:282–288, https://doi.org/10.1016/0146-6313(61)90046-6.

Michaelis, L., and M.L. Menten. 1913. Die kinetik der invertinwirkung. Biochem z 333–369.

Miki, T., and S. Jacquet. 2008. Complex interactions in the microbial world: Under-explored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquatic Microbial Ecology 51:195–208, https://doi.org/10.3354/ame01190.

Mills, E.L. 1989. Biological Oceanography: An Early History, 1870–1960. Cornell University Press, 378 pp.

Moore, C.M., M.M. Mills, A. Milne, R. Langlois, E.P. Achterberg, K. Lochte, R.J. Geider, and J. La Roche. 2006. Iron limits primary productivity during spring bloom development in the central North Atlantic. Global Change Biology 12:626–634, https://doi.org/10.1111/j.1365-2486.2006.01122.x.

Moum, J.N., D.R. Caldwell, and C.A. Paulson. 1989. Mixing in the equatorial surface layer and thermocline. Journal of Geophysical Research 94:2,005–2,022, https://doi.org/10.1029/JC094iC02p02005.

Murphy, G.I. 1971. Clarifying a production model. Limnology and Oceanography 16:981–983, https://doi.org/10.4319/lo.1971.16.6.0981.

Nasmyth, P. 1973. Turbulence and microstructure in the upper ocean. Mémoires de La Société Royale Des Sciences de Liège, Ser. 6, 4:47–56.

Nelson, D., and W. Smith. 1991. Sverdrup revisited: Critical depths, maximum chlorophyll levels, and the control of Southern Ocean productivity by the irradiance-mixing regime. Limnology and Oceanography 36:1,650–1,661, https://doi.org/10.4319/lo.1991.36.8.1650.

Nielsen, E.S. 1958. The balance between phytoplankton and zooplankton in the sea. ICES Journal of Marine Science 23:178–188, https://doi.org/10.1093/icesjms/23.2.178.

Nival, P. 1965. Sur le cycle de dictyocha fibula ehrenberg dans les eaux de surface de la rade de Villefranche-Sur-Mer. Cahiers de Biologie Marine 6:67–82.

Oakey, N.S. 1982. Determination of the rate of dissipation of turbulent energy from simultaneous temperature and velocity shear microstructure measurements. Journal of Physical Oceanography 12:256–271, https://doi.org/10.1175/1520-0485(1982)012<0256:DOTROD>2.0.CO;2.

Oakey, N.S., and J.A. Elliott. 1982. Dissipation within the surface mixed layer. Journal of Physical Oceanography 12:171–185, https://doi.org/10.1175/1520-0485(1982)012<0171:DWTSML>2.0.CO;2.

Obata, A., J. Ishizaka, and M. Endoh. 1996. Global verification of critical depth theory for phytoplankton bloom with climatological in situ temperature and satellite ocean color data. Journal of Geophysical Research 101:20,657–20,667, https://doi.org/10.1029/96JC01734.

Ōkubo, A. 1980. Diffusion and Ecological Problems: Mathematical Models. Springer-Verlag, Berlin-Heidelberg-New York, 254 pp.

Olson, R., and H. Sosik. 2007. A submersible imaging-in-flow instrument to analyze nano- and microplankton: Imaging FlowCytobot. Limnology and Oceanography Methods 5:195–203, https://doi.org/10.4319/lom.2007.5.195.

Osborn, T. 1974. Vertical profiling of velocity microstructure. Journal of Physical Oceanography 4:109–115, https://doi.org/10.1175/1520-0485(1974)004<0109:VPOVM>2.0.CO;2.

Owen, R.W. 1989. Microscale and finescale variations of small plankton in coastal and pelagic environments. Journal of Marine Research 47:197–240, https://doi.org/10.1357/002224089785076415.

Ozmidov, R. 1965. On the turbulent exchange in a stably stratified ocean. Atmospheric and Oceanic Physics 8:853–860.

Platt, T. 1972. Local phytoplankton abundance and turbulence. Deep Sea Research 19:183–187, https://doi.org/10.1016/0011-7471(72)90029-0.

Pomeroy, L.R. 1974. The ocean’s food web, a changing paradigm. BioScience 24:499–504, https://doi.org/10.2307/1296885.

Redfield, A. 1934. On the proportions of organic derivatives in sea water and their relation to the composition of plankton. Pp. 176–192 in James Johnstone Memorial Volume. Liverpool University Press.

Richardson, T.L., and G.A. Jackson. 2007. Small phytoplankton and carbon export from the surface ocean. Science 315:838–840, https://doi.org/10.1126/science.1133471.

Riley, G. 1946. Factors controlling phytoplankton populations on Georges Bank. Journal of Marine Research 6:54–73.

Riley, G., and D. Bumpus. 1946. Phytoplankton-zooplankton relationships on Georges Bank. Journal of Marine Research 6:33–47.

Riser, S.C., and K.S. Johnson. 2008. Net production of oxygen in the subtropical ocean. Nature 451:323–325, https://doi.org/10.1038/nature06441.

Schei, B. 1974. Phytoplankton investigations in Skjomen, a fjord in North Norway, 1970–1971. Astarte 7:17–42.

Scholin, C., G. Massion, E. Mellinger, and M. Brown. 1998. The development and application of molecular probes and novel instrumentation for detection of harmful algae. Ocean Community Conference ’98 Proceedings 1:367–370.

Semina, H. 1960. The influence of vertical circulation on the phytoplankton in the Bering Sea. Internationale Revue Der Gesamten Hydrobiologie 45:1–10, https://doi.org/10.1002/iroh.19600450102.

Siegel, D., S. Doney, and J. Yoder. 2002. The North Atlantic spring phytoplankton bloom and Sverdrup’s critical depth hypothesis. Science 296:730–733, https://doi.org/10.1126/science.1069174.

Skellam, J. 1951. Random dispersal in theoretical populations. Biometrika 38:196–218.

Smetacek, V., and U. Passow. 1990. Spring bloom initiation and Sverdrup’s critical-depth model. Limnology and Oceanography 35:228–234, https://doi.org/10.4319/lo.1990.35.1.0228.

Steele, J.H. 1962. Environmental control of photosynthesis in the sea. Limnology and Oceanography 7:137–150, https://doi.org/10.4319/lo.1962.7.2.0137.

Steele, J.H., and D.W. Menzel. 1962. Conditions for maximum primary production in the mixed layer. Deep Sea Research 9:39–49, https://doi.org/10.1016/0011-7471(62)90245-0.

Stramska, M., and T.D. Dickey. 1994. Modeling phytoplankton dynamics in the Northeast Atlantic during the initiation of the spring bloom. Journal of Geophysical Research 99:10,241–10,253, https://doi.org/10.1029/93JC03378.

Strom, S., M. Brainard, J. Holmes, and M. Olson. 2001. Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Marine Biology 138:355–368, https://doi.org/10.1007/s002270000461.

Strom, S.L., C.B. Miller, and B.W. Frost. 2000. What sets lower limits to phytoplankton stocks in high-nitrate, low-chlorophyll regions of the open ocean? Marine Ecology Progress Series 193:19–31, https://doi.org/10.3354/meps193019.

Sverdrup, H. 1953. On conditions for the vernal blooming of phytoplankton. Journal du Conseil International pour l’Exploration de la Mer 18:287–295, https://doi.org/10.1093/icesjms/18.3.287.

Taylor, J., and R. Ferrari. 2011. Shutdown of turbulent convection as a new criterion for the onset of spring phytoplankton blooms. Limnology and Oceanography 56:2,293–2,307, https://doi.org/10.4319/lo.2011.56.6.2293.

Thomas, C.W. 1966. Vertical circulation off Ross Ice Shelf. Pacific Science 20:239–245.

Thorpe, S. 1977. Turbulence and mixing in a Scottish loch. Philosophical Transactions for the Royal Society of London. Series A 286:125–181, https://doi.org/10.1098/rsta.1977.0112.

Thorpe, S. 2005. The Turbulent Ocean. Cambridge University Press, New York, NY, 439 pp.

Tilzer, M.M., and C.R. Goldman. 1978. Importance of mixing, thermal stratification and light adaptation for phytoplankton productivity in Lake Tahoe (California-Nevada). Ecology 59:810–821, https://doi.org/10.2307/1938785.

Townsend, D.W., M.D. Keller, M.E. Sieracki, and S.G. Ackleson. 1992. Spring phytoplankton blooms in the absence of vertical water column stratification. Nature 360:59–62, https://doi.org/10.1038/360059a0.

Venrick, E.L., J.A. McGowan, D.R. Cayan, and T.L. Hayward. 1987. Climate and chlorophyll a: Long-term trends in the Central North Pacific Ocean. Science 238:70–72, https://doi.org/10.1126/science.238.4823.70.

Walsh, J.J. 1971. Relative importance of habitat variables in predicting distribution of phytoplankton at ecotone of Antarctic upwelling ecosystem. Ecological Monographs 41:291–309, https://doi.org/10.2307/1948495.

Yoder, J., and C. McClain. 1993. Annual cycles of phytoplankton chlorophyll concentrations in the global ocean: A satellite view. Global Biogeochemical Cycles 7:181–193, https://doi.org/10.1029/93GB02358.

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.