Where Light and Nutrients Collide: The Global Distribution and Activity of Subsurface Chlorophyll Maximum Layers

  • Greg M. SilsbeEmail author
  • Sairah Y. Malkin


A satellite view of the world’s oceans presents a mosaic of high chlorophyll (Chla) regions adjacent vast Chla deserts. However, such a view is limited because it reflects conditions of near surface waters only, and misses the vast and sometimes permanent regions of elevated Chla that can exist in subsurface waters. Subsurface chlorophyll maximum layers (SCMLs) are widespread features of the global ocean and are composed of phytoplankton communities that are chromatically and nutritionally adapted to these environments. In this chapter, we first outline the drivers that structure the formation and persistence of SCMLs in marine systems. We develop a simple model that predicts the global distribution and seasonal persistence of SCMLs and find that during any given season, between 59 and 73 % of the ocean may support an SCML. Using a well established global net primary production model, we further predict that approximately 47 % of ocean primary production occurs within SCMLs, a surprisingly large fraction, given the degree of light limitation at these depths. For context, we synthesize key works that have investigated primary production, phytoplankton biomass, and/or nutrient turnover within SCMLs across a range of ocean biomes. These recent studies support previous hypotheses that SCMLs are important sites for new production, and indicate that this new production largely occurs during times when SCMLs are moving deeper into nutriclines or when they are supplied with nutrients through other mechanisms (e.g., tides). In a final section, we draw upon our formative studies in limnology to make linkages between marine and lacustrine systems in terms of the structure and function of SCMLs. Because of large gradients in size, optical properties, and nutritional status across lakes, these systems may present ideal environments to test hypotheses related to the regulation and consequences of SCML productivity.


Deep chlorophyll maximum Phytoplankton Primary production Photoacclimation 



We wish to thank our past and present mentors, particularly Bob Hecky and Stephanie Guildford, for encouraging us through our careers. We also extend our appreciation to Sébastien Gardoll for a brief residency in Paris, to formulate the ideas that became this chapter. Data and the model code of Westberry et al. (2008) were obtained from the NASA-funded Oregon State University Ocean Productivity project (


  1. Abbott MR, Denman KL, Powell TM, Richerson PJ, Richards RC, Goldman CR (1984) Mixing and the dynamics of the deep chlorophyll maximum in Lake Tahoe. Limnol Oceanogr 29:862–878. doi: 10.4319/lo.1984.29.4.0862 CrossRefGoogle Scholar
  2. Arrigo KR, Matrai PA, van Dijken GL (2011) Primary productivity in the Arctic Ocean: impacts of complex optical properties and subsurface chlorophyll maxima on large-scale estimates. J Geophys Res: Oceans 116, C11022. doi: 10.1029/2011JC007273 CrossRefGoogle Scholar
  3. Barbeiro RP, Tuchman ML (2001) Results from the U.S. EPA’s biological open water surveillance program of the Laurentian great lakes: II. Deep chlorophyll maxima J. Great Lakes Res 27:155–166. doi: 10.1016/S0380-1330(01)70629-6 CrossRefGoogle Scholar
  4. Cullen JJ (2014) Subsurface chlorophyll maximum layers: enduring enigma or mystery solved? Ann Rev Mar Sci 7:19.1–19.33. doi: 10.1146/annurev-marine-010213-135111 Google Scholar
  5. Dugdale RC, Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr 12:196–206. doi: 10.4319/lo.1967.12.2.0196 CrossRefGoogle Scholar
  6. Estrada M (1996) Primary production in the northwestern Mediterranean. Sci Mar 60(Suppl 2):55–64Google Scholar
  7. Fahnenstiel GL, Scavia D (1987) Dynamics of lake Michigan phytoplankton: the deep chlorophyll layer. J Great Lakes Res 13:285–295. doi: 10.1016/S0380-1330(87)71652-9 CrossRefGoogle Scholar
  8. Fairbanks RG, Weibe PH (1980) Foraminifera and chlorophyll maximum: vertical distribution, seasonal succession, and paleoceanographic significance. Science 209:1524–1526. doi: 10.1126/science.209.4464.1524 CrossRefPubMedGoogle Scholar
  9. Fennel K, Boss E (2003) Subsurface maxima of phytoplankton and chlorophyll: steady-state solutions from a simple model. Limnol Oceanogr 48:1521–1534. doi: 10.4319/lo.2003.48.4.1521 CrossRefGoogle Scholar
  10. Francis TB, Schindler DE, Holtgrieve GW, Larson ER, Scheuerell MD, Semmens BX, Ward EJ (2011) Habitat structure determines resource use by zooplankton in temperate lakes. Ecol Lett 14:364–372. doi: 10.1111/j.1461-0248.2011.01597.x CrossRefPubMedGoogle Scholar
  11. Geider RJ, MacIntyre HL, Kana TM (1998) A dynamic regulatory model of phytoplankton acclimation to light, nutrients and temperature. Limnol Oceanogr 43:679–694. doi: 10.4319/lo.1998.43.4.0679 CrossRefGoogle Scholar
  12. Hickman AE, Holligan PM, Moore CM, Sharples J, Krivtsov V, Palmer MR (2009) Distribution and chromatic adaptation of phytoplankton within a shelf sea thermocline. Limnol Oceanogr 54:525–536. doi: 10.4319/lo.2009.54.2.0525 CrossRefGoogle Scholar
  13. Hickman AE, Moore CM, Sharples J, Lucas MI, Tilstone GH, Krivtsov V, Holligan PM (2012) Primary production and nitrate uptake within the seasonal thermocline of a stratified shelf sea. Mar Ecol Prog Ser 463:39–57. doi: 10.3354/meps09836 CrossRefGoogle Scholar
  14. Hodges BA, Rudnick DL (2004) Simple models of steady deep maxima in chlorophyll and biomass. Deep-Sea Res Part I 51:999–1015. doi: 10.1016/j.dsr.2004.02.009 CrossRefGoogle Scholar
  15. Johnson KS, Riser SC, Karl DM (2010) Nitrate supply from deep to near-surface waters of the North Pacific subtropical gyre. Nature 465:1062–1065. doi: 10.1038/nature09170 CrossRefPubMedGoogle Scholar
  16. Klausmeier CA, Litchman E (2001) Algal games: the vertical distribution of phytoplankton in poorly mixed water columns. Limnol Oceanogr 46:1998–2007. doi: 10.4319/lo.2001.46.8.1998 CrossRefGoogle Scholar
  17. Letelier RM, Karl DM, Abbot MR, Bidagare RR (2004) Light driven seasonal patterns of chlorophyll and nitrate in the lower euphotic zone of the North Pacific Subtropical Gyre. Limnol Oceanogr 49:508–519. doi: 10.4319/lo.2004.49.2.0508 CrossRefGoogle Scholar
  18. Malkin SY, Silsbe GM, Smith REH, Howell ET (2012) A deep chlorophyll maximum nourishes benthic filter feeders in the coastal zone of a large clear lake. Limnol Oceanogr 57:735–748. doi: 10.4319/lo.2012.57.3.0735 CrossRefGoogle Scholar
  19. Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J, Zinser ER, Chisholm SW (2010) Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J 4:1252–1264. doi: 10.1038/ismej.2010.60 CrossRefPubMedGoogle Scholar
  20. Martin J, Tremblay J-É, Gagnon J, Tremblay G, Lapoussière A, Jose C, Poulin M, Gosselin M, Gratton Y, Michel C (2010) Prevalence, structure and properties of subsurface chlorophyll maxima in Canadian Arctic waters. Mar Ecol Prog Ser 412:69–84. doi: 10.3354/meps08666 CrossRefGoogle Scholar
  21. Martin J, Tremblay J-É, Price NM (2012) Nutritive and photosynthetic ecology of subsurface chlorophyll maxima in Canadian Arctic waters. Biogeosciences 9:5353–5371. doi: 10.5194/bg-9-5353-2012 CrossRefGoogle Scholar
  22. Mignot A, Claustre H, Uitz J, Poteau A, D’Ortenzio F, Xing X (2014) Understanding the seasonal dynamics of phytoplankton biomass and the deep chlorophyll maximum in oligotrophic environments: A Bio-Argo float investigation. Global Biogeochem Cycles 28:856–876. doi: 10.1002/2013GB004781 CrossRefGoogle Scholar
  23. Moll RA, Brahce MZ, Peterson TP (1984) Phytoplankton dynamics within the subsurface chlorophyll maximum of Lake Michigan. J Plankton Res 6:751–766. doi: 10.1093/plankt/6.5.751 CrossRefGoogle Scholar
  24. Moore LM, Chisholm SW (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: Ecotypic differences among cultured isolates. Limnol Oceanogr 44:628–638. doi: 10.4319/lo.1999.44.3.0628 CrossRefGoogle Scholar
  25. Moore CM, Suggett DJ, Hickman AE, Kim Y-N, Tweddle JF, Sharples J, Geider RJ, Holligan PM (2006) Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnol Oceanogr 51:936–949. doi: 10.4319/lo.2006.51.2.0936 CrossRefGoogle Scholar
  26. Nalepa TF, Fanslow DL, Lang GA (2009) Transformation of the offshore benthic community in Lake Michigan: recent shift from the native amphipod Diporeia spp. to the invasive mussel Dreissena rostriformis bugensis. Freshwater Biol 54:466–479. doi: 10.1111/j.1365-2427.2008.02123.x CrossRefGoogle Scholar
  27. Pannard A, Beisner BE, Bird DF, Braun J, Planas D, Bormans M (2011) Recurrent internal waves in a small lake: Potential ecological consequences for metalimnetic phytoplankton populations. Limnol Oceanogr: Fluids Environ 1:91–109. doi: 10.1215/21573698-1303296 CrossRefGoogle Scholar
  28. Richardson K, Visser AW, Pedersen FB (2000) Subsurface phytoplankton blooms fuel pelagic production in the North Sea. J Plankton Res 22:1663–1671. doi: 10.1093/plankt/22.9.1663 CrossRefGoogle Scholar
  29. Saba VS, Friedrichs MA, Carr M-E, Antoine D, Armstrong RA et al (2011) Challenges of modeling depth‐integrated marine primary productivity over multiple decades: A case study at BATS and HOT. Glob Biogeochem Cycles 24, GB3020. doi: 10.1029/2009GB003655 Google Scholar
  30. Seki MP, Polovina JJ, Brainard RE, Bidigare RR, Leonard CL, Foley DG (2001) Biological enhancement at cyclonic eddies tracked with GOES thermal imagery in Hawaiian waters. Geophys Res Lett 28:1583–1586. doi: 10.1029/2000GL012439 CrossRefGoogle Scholar
  31. Silsbe GM, Smith REH, Hecky RE (2012) Improved estimation of carbon fixation rates from active fluorometry using spectral fluorescence in light-limited environments. Limnol Oceanogr Methods 10:736–751. doi: 10.4319/lom.2012.10.736 CrossRefGoogle Scholar
  32. Tittel J, Bissinger V, Zippel B, Gaedke U, Bell E, Lorke A, Kamjunke N (2003) Mixotrophs combine resource use to outcompete specialists: Implications for aquatic food webs. Proc Natl Acad Sci U S A 100:12776–12781. doi: 10.1073/pnas.2130696100 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Uitz J, Claustre H, Morel A, Hooker SB (2006) Vertical distribution of phytoplankton communities in open ocean: an assessment based on surface chlorophyll. J Geophys Res 111:C08005. doi: 10.1029/2005JC003207 CrossRefGoogle Scholar
  34. Venrick EL (1988) The vertical distributions of chlorophyll and phytoplankton species in the North Pacific central environment. J Plankton Res 10:987–998. doi: 10.1093/plankt/10.5.987 CrossRefGoogle Scholar
  35. Villareal TA, Pilskaln CH, Montoya JP, Dennet M (2014) Upward nitrate transport by phytoplankton in oceanic waters: balancing nutrient budgets in oligotrophic seas. Peer J 2, e302. doi: 10.7717/peerj.302 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Westberry T, Behrenfeld MJ, Siegel DA, Boss E (2008) Carbon-based primary productivity modelling with vertically resolved photoacclimation. Global Biogeochem Cycles 22:1–18. doi: 10.1029/2007GB003078 CrossRefGoogle Scholar
  37. Williams C, Sharples J, Green M, Mahaffey C, Rippeth T (2013) The maintenance of the subsurface chlorophyll maximum in the stratified western Irish Sea. Limnol. Oceanogr: Fluids Environ 3:61–73. doi: 10.1215/21573689-2285100 Google Scholar
  38. Williamson CE, Sanders RW, Moeller RE, Stutzman PL (1996) Utilization of subsurface food resources for zooplankton reproduction: Implications for diel vertical migration theory. Limnol Oceanogr 41:224–233. doi: 10.4319/lo.1996.41.2.0224 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Horn Point LaboratoryUniversity of Maryland Center for Environmental ScienceCambridgeUSA
  2. 2.Department of Botany and Plant PathologyOregon State University (OSU)CorvallisUSA
  3. 3.Department of Marine SciencesUniversity of GeorgiaAthensUSA

Personalised recommendations