Log in

Marine Ecosystems as Complex Adaptive Systems: Emergent Patterns, Critical Transitions, and Public Goods

  • 20th Anniversary Paper
  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Complex adaptive systems provide a unified framework for explaining ecosystem phenomena. In the past 20 years, complex adaptive systems have been sharpened from an abstract concept into a series of tools that can be used to solve concrete problems. These advances have been led by the development of new techniques for coupling ecological and evolutionary dynamics, for integrating dynamics across multiple scales of organization, and for using data to infer the complex interactions among different components of ecological systems. Focusing on the development and usage of these new methods, we discuss how they have led to an improved understanding of three universal features of complex adaptive systems, emergent patterns; tip** points and critical phenomena; and cooperative behavior. We restrict our attention primarily to marine ecosystems, which provide numerous successful examples of the application of complex adaptive systems. Many of these are currently undergoing dramatic changes due to anthropogenic perturbations, and we take the opportunity to discuss how complex adaptive systems can be used to improve the management of public goods and to better preserve critical ecosystem services.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Almany G, Connolly S, Heath D, Hogan J, Jones G, McCook L, Mills M, Pressey R, Williamson D. 2009. Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28(2):339–51.

    Article  Google Scholar 

  • Andersen KH, Berge T, Gonçalves R, Hartvig M, Heuschele J, Hylander S, Jacobsen NS, Lindemann C, Martens EA, Neuheimer AB et al. 2016. Characteristic sizes of life in the oceans, from bacteria to whales. Annu Rev Mar Sci 8(2016):217–41.

    Article  CAS  Google Scholar 

  • Anderson PW. 1972. More is different. Science 177(4047):393–6.

    Article  CAS  PubMed  Google Scholar 

  • Armstrong RA. 1994. Grazing limitation and nutrient limitation in marine ecosystems: steady state solutions of an ecosystem model with multiple food chains. Limnol Oceanogr 39(3):597–608.

    Article  CAS  Google Scholar 

  • Arrow KJ, Cropper ML, Gollier C, Groom B, Heal GM, Newell RG, Nordhaus WD, Pindyck RS, Pizer WA, Portney PR et al. 2014. Should governments use a declining discount rate in project analysis? Rev Environ Econ Policy 8(2):145–63.

    Article  Google Scholar 

  • Arthur WB. 1994. Increasing returns and path dependence in the economy. Ann Arbor (MI): University of Michigan Press. p 203.

    Google Scholar 

  • Axelrod RM. 2006. The evolution of cooperation. New York (NY): Basic books. p 247.

    Google Scholar 

  • Bak P, Tang C, Wiesenfeld K. 1987. Self-organized criticality: an explanation of the 1/f noise. Phys Rev Lett 59(4):381.

    Article  CAS  PubMed  Google Scholar 

  • Berdahl A, Torney CJ, Ioannou CC, Faria JJ, Couzin ID. 2013. Emergent sensing of complex environments by mobile animal groups. Science 339(6119):574–6.

    Article  CAS  PubMed  Google Scholar 

  • Berry D, Widder S. 2014. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bialek W, Cavagna A, Giardina I, Mora T, Silvestri E, Viale M, Walczak AM. 2012. Statistical mechanics for natural flocks of birds. Proc Natl Acad Sci 109(13):4786–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boettiger C, Hastings A. 2012a. Early warning signals and the prosecutor’s fallacy. Proc R Soc Lond B Biol Sci 279(1748):2085.

  • Boettiger C, Hastings A. 2012b. Quantifying limits to detection of early warning for critical transitions. J R Soc Interface 9(75):2527–39.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruggeman J. 2011. A phylogenetic approach to the estimation of phytoplankton traits. J Phycol 47(1):52–65.

    Article  PubMed  Google Scholar 

  • Brush ER, Leonard NE, Levin SA. 2016. The content and availability of information affects the evolution of social-information gathering strategies. Theor Ecol 9:455–76.

    Google Scholar 

  • Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, No D, Liu H, Kinnebrew M, Viale A et al. 2015. Precision microbiome reconstitution restores bile acid mediated resistance to clostridium difficile. Nature 517(7533):205–8.

    Article  CAS  PubMed  Google Scholar 

  • Bunin G. 2016. Interaction patterns and diversity in assembled ecological communities. ar**v preprint ar**v:1607.04734.

  • Carpenter SR, Brock WA. 2006. Rising variance: a leading indicator of ecological transition. Ecol Lett 9(3):311–18.

    Article  CAS  PubMed  Google Scholar 

  • Carpenter SR, Ludwig D, Brock WA. 1999. Management of eutrophication for lakes subject to potentially irreversible change. Ecol Appl 9(3):751–71.

    Article  Google Scholar 

  • Carpenter SR, Press MC, Huntly NJ, Levin SA. 2001. Alternate states of ecosystems: evidence and some implications. In: Ecology: achievement and challenge: the 41st symposium of the British Ecological Society sponsored by the Ecological Society of America held at Orlando, Florida, USA, 10–13 April 2000, pp. 357–83.

  • Cavagna A, Cimarelli A, Giardina I, Parisi G, Santagati R, Stefanini F, Viale M. 2010. Scale-free correlations in starling flocks. Proc Natl Acad Sci 107(26):11865–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman S, Cowling TG. 1970. The mathematical theory of non-uniform gases: an account of the kinetic theory of viscosity, thermal conduction and diffusion in gases. Cambridge (UK): Cambridge University Press.

    Google Scholar 

  • Clark JR, Lenton TM, Williams HT, Daines SJ. 2013. Environmental selection and resource allocation determine spatial patterns in picophytoplankton cell size. Limnol Oceanogr 58(3):1008–22.

    Article  Google Scholar 

  • Clauset A, Shalizi CR, Newman ME. 2009. Power-law distributions in empirical data. SIAM Rev 51(4):661–703.

    Article  Google Scholar 

  • Cordero OX, Ventouras LA, DeLong EF, Polz MF. 2012. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc Natl Acad Sci 109(49):20059–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couzin ID, Krause J. 2003. Self-organization and collective behavior in vertebrates. Adv Study Behav 32:1–75.

    Article  Google Scholar 

  • Couzin ID, Krause J, Franks NR, Levin SA. 2005. Effective leadership and decision-making in animal groups on the move. Nature 433(7025):513–16.

    Article  CAS  PubMed  Google Scholar 

  • Crépin AS. 2007. Using fast and slow processes to manage resources with thresholds. Environ Resour Econ 36(2):191–213.

    Article  Google Scholar 

  • Czirók A, Vicsek T. 2001. Collective motion. In: Vicsek T (ed) Fluctuations and scaling in biology. Oxford (UK): Oxford University Press. pp. 177–242.

  • Daines SJ, Clark JR, Lenton TM. 2014. Multiple environmental controls on phytoplankton growth strategies determine adaptive responses of the N:P ratio. Ecol Lett 17(4):414–25.

    Article  PubMed  Google Scholar 

  • Damore JA, Gore J. 2012. Understanding microbial cooperation. J Theor Biol 299:31–41.

    Article  PubMed  Google Scholar 

  • Darwin C. 1859. The origin of species. London (UK): Murray, pp. 495.

  • Datta MS, Sliwerska E, Gore J, Polz MF, Cordero OX. 2016. Microbial interactions lead to rapid micro-scale successions on model marine particles. Nat Commun 7:11965. doi:10.1038/ncomms11965.

  • Diaz RJ, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321(5891):926–9.

    Article  CAS  PubMed  Google Scholar 

  • Diekmann O. 2004. A beginner’s guide to adaptive dynamics. Banach Center Publ 63:47–86.

  • Dietz T. 2005. The Darwinian trope in the drama of the commons: variations on some themes by the Ostroms. J Econ Behav Organ 57(2):205–25.

    Article  Google Scholar 

  • Dietz T, Ostrom E, Stern PC. 2003. The struggle to govern the commons. Science 302(5652):1907–12.

    Article  CAS  PubMed  Google Scholar 

  • Drescher K, Dunkel J, Nadell CD, van Teeffelen S, Grnja I, Wingreen NS, Stone HA, Bassler BL. 2016. Architectural transitions in vibrio cholerae biofilms at single-cell resolution. Proc Natl Acad Sci 113(14):E2066–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Driscoll WW, Pepper JW. 2010. Theory for the evolution of diffusible external goods. Evolution 64(9):2682–7.

    Article  PubMed  Google Scholar 

  • Drossel B, McKane AJ, Quince C. 2004. The impact of nonlinear functional responses on the long-term evolution of food web structure. J Theor Biol 229(4):539–48.

    Article  PubMed  Google Scholar 

  • Dunne JA, Williams RJ, Martinez ND. 2002. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5(4):558–67.

    Article  Google Scholar 

  • Eikeset AM, Richter A, Dunlop ES, Dieckmann U, Stenseth NC. 2013. Economic repercussions of fisheries-induced evolution. Proc Natl Acad Sci 110(30):12259–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enquist BJ, Norberg J, Bonser SP, Violle C, Webb CT, Henderson A, Sloat LL, Savage VM. 2015. Chapter nine-scaling from traits to ecosystems: develo** a general trait driver theory via integrating trait-based and metabolic scaling theories. Adv Ecol Res 52:249–318.

    Article  Google Scholar 

  • Falkowski PG. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387(6630):272–5.

    Article  CAS  Google Scholar 

  • Falkowski PG, Fenchel T, Delong EF. 2008. The microbial engines that drive earth’s biogeochemical cycles. Science 320(5879):1034–9.

    Article  CAS  PubMed  Google Scholar 

  • Fenichel N. 1979. Geometric singular perturbation theory for ordinary differential equations. J Differ Equ 31(1):53–98.

    Article  Google Scholar 

  • Filotas E, Parrott L, Burton PJ, Chazdon RL, Coates DK, Coll L, Haeussler S, Martin K, Nocentini S, Puettmann KJ. 2014. Viewing forests through the lens of complex systems science. Ecosphere 5(1):1–23.

    Article  Google Scholar 

  • Flierl G, Grünbaum D, Levin SA, Olson D. 1999. From individuals to aggregations: the interplay between behavior and physics. J Theor Biol 196(4):397–454.

    Article  CAS  PubMed  Google Scholar 

  • Follows MJ, Dutkiewicz S, Grant S, Chisholm SW. 2007. Emergent biogeography of microbial communities in a model ocean. Science 315(5820):1843–6.

    Article  CAS  PubMed  Google Scholar 

  • Franks PJS. 2009. Planktonic ecosystem models: perplexing parameterizations and a failure to fail. J Plankton Res 31:1299–306.

    Article  Google Scholar 

  • Fulton EA, Smith AD, Smith DC, van Putten IE. 2011. Human behaviour: the key source of uncertainty in fisheries management. Fish Fish 12(1):2–17.

    Article  Google Scholar 

  • Galbraith ED, Martiny AC. 2015. A simple nutrient-dependence mechanism for predicting the stoichiometry of marine ecosystems. Proc Natl Acad Sci 112(27):8199–204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardiner CW. 1985. Handbook of stochastic methods, Vol. 3Berlin (DEU): Springer.

    Google Scholar 

  • Gattuso JP, Magnan A, Billé R, Cheung WWL, Howes EL, Joos F, Allemand D, Bopp L, Cooley SR, Eakin CM, Hoegh-Guldberg O, Kelly RP, Pörtner HO, Rogers AD, Baxter JM, Laffoley D, Osborn D, Rankovic A, Rochette J, Sumaila UR, Treyer S, Turley C. 2015. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349(6243):aac4722. doi:10.1126/science.aac4722.

  • Geritz SA, Metz JA, Kisdi É, Meszéna G. 1997. Dynamics of adaptation and evolutionary branching. Phys Rev Lett 78(10):2024.

    Article  CAS  Google Scholar 

  • Gore J, Youk H, Van Oudenaarden A. 2009. Snowdrift game dynamics and facultative cheating in yeast. Nature 459(7244):253–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimm V, Railsback SF. 2013. Individual-based modeling and ecology. Princeton (NJ): Princeton University Press.

    Google Scholar 

  • Grünbaum D. 1994. Translating stochastic density-dependent individual behavior with sensory constraints to an Eulerian model of animal swarming. J Math Biol 33(2):139–61.

    Article  PubMed  Google Scholar 

  • Grünbaum D. 1998. Schooling as a strategy for taxis in a noisy environment. Evol Ecol 12(5):503–22.

    Article  Google Scholar 

  • Grünbaum D, Okubo A. 1994. Modelling social animal aggregations. In Frontiers in mathematical biology. Berlin (DEU): Springer. pp. 296–325.

  • Gunderson LH. 2001. Panarchy: understanding transformations in human and natural systems. Washington (DC): Island Press.

    Google Scholar 

  • Guttal V, Jayaprakash C. 2008. Changing skewness: an early warning signal of regime shifts in ecosystems. Ecol Lett 11(5):450–60.

    Article  PubMed  Google Scholar 

  • Hagstrom GI, Levin SA, Martiny AC. 2016. Balance between resource supply and demand determines nutrient limitation of primary productivity in the ocean. doi:10.1101/064543.

  • Hartvigsen G, Kinzig A, Peterson G. 1998. Complex adaptive systems: use and analysis of complex adaptive systems in ecosystem science: overview of special section. Ecosystems 1(5):427–30.

    Article  Google Scholar 

  • Hein A, Rosenthal SB, Hagstrom G, Berdahl A, Torney C, Couzin I. 2015. The evolution of distributed sensing and collective computation in animal populations. eLife 4:10955.

    Article  Google Scholar 

  • Heino M. 1998. Management of evolving fish stocks. Can J Fish Aquat Sci 55(8):1971–82.

    Article  Google Scholar 

  • Held H, Kleinen T. 2004. Detection of climate system bifurcations by degenerate fingerprinting. Geophys Res Lett 31(23). doi:10.1029/2004GL020972.

  • Holling CS. 1973. Resilience and stability of ecological systems. Annu Rev Ecol Syst 4:1–23.

  • Holling CS. 1986. The resilience of terrestrial ecosystems: local surprise and global change. In: Clark WC, Seliger HH (eds) Sustainable development of the biosphere. Cambridge (UK): Cambridge University Press. pp. 292–317.

  • Jacob F. 1977. Evolution and tinkering. Science 196(4295):1161–6.

    Article  CAS  PubMed  Google Scholar 

  • Katz Y, Tunstrøm K, Ioannou CC, Huepe C, Couzin ID. 2011. Inferring the structure and dynamics of interactions in schooling fish. Proc Natl Acad Sci 108(46):18720–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khandelwal RA, Olivier BG, Röling WF, Teusink B, Bruggeman FJ. 2013. Community flux balance analysis for microbial consortia at balanced growth. PLoS ONE 8(5):e64567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiørboe T. 1993. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv Mar Biol 29:1–72.

    Article  Google Scholar 

  • Klausmeier CA, Litchman E, Daufresne T, Levin SA. 2004. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429(6988):171–4.

    Article  CAS  PubMed  Google Scholar 

  • Knowlton N. 1992. Thresholds and multiple stable states in coral reef community dynamics. Am Zool 32(6):674–82.

    Article  Google Scholar 

  • Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. 2015. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol 11(5):e1004226.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lenton TM. 2011. Early warning of climate tip** points. Nat Clim Change 1(4):201–9.

    Article  Google Scholar 

  • Lenton TM, Footitt A, Dlugolecki A, Allianz Gruppe. 2009. Major tip** points in the earth’s climate system and consequences for the insurance sector. Technical report, World Wildlife Fund, Washington (DC).

  • Levin S. 2003. Complex adaptive systems: exploring the known, the unknown and the unknowable. Bull Am Math Soc 40(1):3–19.

    Article  Google Scholar 

  • Levin S, Xepapadeas T, Crépin AS, Norberg J, De Zeeuw A, Folke C, Hughes T, Arrow K, Barrett S, Daily G et al. 2013. Social-ecological systems as complex adaptive systems: modeling and policy implications. Environ Dev Econ 18(02):111–32.

    Article  Google Scholar 

  • Levin SA. 1992. The problem of pattern and scale in ecology: the Robert H. MacArthur Award lecture. Ecology 73(6):1943–67.

    Article  Google Scholar 

  • Levin SA. 1998. Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1(5):431–6.

    Article  Google Scholar 

  • Levin SA. 2014. Public goods in relation to competition, cooperation, and spite. Proc Natl Acad Sci 111(Supplement 3):10838–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levin SA, Barrett S, Aniyar S, Baumol W, Bliss C, Bolin B, Dasgupta P, Ehrlich P, Folke C, Gren IM et al. 1998. Resilience in natural and socioeconomic systems. Environ Dev Econ 3(02):221–62.

    Article  Google Scholar 

  • Levin SA, Lubchenco J. 2008. Resilience, robustness, and marine ecosystem-based management. Bioscience 58(1):27–32.

    Article  Google Scholar 

  • Litchman E, Klausmeier CA. 2008. Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639.

  • Lomas MW, Bonachela JA, Levin SA, Martiny AC. 2014. Impact of ocean phytoplankton diversity on phosphate uptake. Proc Natl Acad Sci 111(49):17540–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margalef R, Miyares ME, de Rubinat DBF. 1979. Functional morphology of organisms involved in red tides, as adapted to decaying turbulence. In: Toxic and dinoflagellate blooms. Amsterdam (NL): Elsevier.

  • Martín PV, Bonachela JA, Levin SA, Muñoz MA. 2015. Eluding catastrophic shifts. Proc Natl Acad Sci 112(15):E1828–36.

    Article  CAS  Google Scholar 

  • Martiny AC, Pham CTA, Primeau FW, Vrugt JA, Moore JK, Levin SA, Lomas MW. 2013. Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat Geosci 6(4):279–83.

    Article  CAS  Google Scholar 

  • May RM. 1977. Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature 269(5628):471–7.

    Article  Google Scholar 

  • May RM, Levin SA, Sugihara G. 2008. Complex systems: ecology for bankers. Nature 451(7181):893–5.

    Article  CAS  PubMed  Google Scholar 

  • Merico A, Bruggeman J, Wirtz K. 2009. A trait-based approach for downscaling complexity in plankton ecosystem models. Ecol Model 220(21):3001–10.

    Article  CAS  Google Scholar 

  • Messier C, Puettmann K, Chazdon R, Andersson KP, Angers VA, Brotons L, Filotas E, Tittler R, Parrott L, Levin SA. 2015. From management to stewardship: viewing forests as complex adaptive systems in an uncertain world. Conserv Lett 8(5):368–77.

    Article  Google Scholar 

  • Momeni B, Waite AJ, Shou W. 2013. Spatial self-organization favors heterotypic cooperation over cheating. eLife 2:e00960.

    PubMed  PubMed Central  Google Scholar 

  • Montoya JM, Pimm SL, Solé RV. 2006. Ecological networks and their fragility. Nature 442(7100):259–64.

    Article  CAS  PubMed  Google Scholar 

  • Mora T, Bialek W. 2011. Are biological systems poised at criticality? J Stat Phys 144(2):268–302.

    Article  Google Scholar 

  • Morris JJ, Lenski RE, Zinser ER. 2012. The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3(2):e00036.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mueller T, Fagan WF. 2008. Search and navigation in dynamic environments–from individual behaviors to population distributions. Oikos 117(5):654–64.

    Article  Google Scholar 

  • Murray JD. 2002. Mathematical biology I: an introduction. In: Antman SS, Marsden JE, Sirovich L, Wiggins S (eds) Interdisciplinary applied mathematics, Vol. 17. New York (NY): Springer.

  • Nadell CD, Bucci V, Drescher K, Levin SA, Bassler BL, Xavier JB. 2013. Cutting through the complexity of cell collectives. Proc R Soc B 280(1755):20122770.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nadell CD, Drescher K, Wingreen NS, Bassler BL. 2015. Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J 9(8):1700–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nadell CD, Foster KR, Xavier JB. 2010. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 6(3):e1000716.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nadell CD, Xavier JB, Levin SA, Foster KR. 2008. The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6(1):e14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Newman ME. 2003. The structure and function of complex networks. SIAM Rev 45(2):167–256.

    Article  Google Scholar 

  • Norberg J. 2004. Biodiversity and ecosystem functioning: a complex adaptive systems approach. Limnol Oceanogr 49(4):1269–77.

    Article  Google Scholar 

  • Norberg J, Swaney DP, Dushoff J, Lin J, Casagrandi R, Levin SA. 2001. Phenotypic diversity and ecosystem functioning in changing environments: a theoretical framework. Proc Natl Acad Sci 98(20):11376–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ostrom E. 1990. Governing the commons: the evolution of institutions for collective action. Cambridge (UK): Cambridge University Press.

    Book  Google Scholar 

  • Ostrom E. 2010. Polycentric systems for co** with collective action and global environmental change. Glob Environ Change 20(4):550–7.

    Article  Google Scholar 

  • Pacala SW, Silander J. 1985. Neighborhood models of plant population dynamics. I. Single-species models of annuals. Am Nat 125(3):385–411.

  • Paine RT. 1969. A note on trophic complexity and community stability. Am Nat 103(929):91–3.

    Article  Google Scholar 

  • Pascual M, Guichard F. 2005. Criticality and disturbance in spatial ecological systems. Trends Ecol Evol 20(2):88–95.

    Article  PubMed  Google Scholar 

  • Pascual M, Roy M, Guichard F, Flierl G. 2002. Cluster size distributions: signatures of self–organization in spatial ecologies. Philos Trans R Soc Lond B Biol Sci 357(1421):657–66.

    Article  PubMed  PubMed Central  Google Scholar 

  • Picioreanu C, Van Loosdrecht MC, Heijnen JJ et al. 1998. Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol Bioeng 58(1):101–16.

    Article  CAS  PubMed  Google Scholar 

  • Pinsky ML, Palumbi SR. 2014. Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23(1):29–39.

    Article  PubMed  Google Scholar 

  • Polasky S, Carpenter SR, Folke C, Keeler B. 2011. Decision-making under great uncertainty: environmental management in an era of global change. Trends Ecol Evol 26(8):398–404.

    Article  PubMed  Google Scholar 

  • Rakoff-Nahoum S, Coyne MJ, Comstock LE. 2014. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol 24(1):40–9.

    Article  CAS  PubMed  Google Scholar 

  • Redfield AC. 1958. The biological control of chemical factors in the environment. Am Sci 46(3):230A, 205–21.

  • Rodriguez-Iturbe I, Rinaldo A. 1997. Fractal river networks: chance and self-organization. New York (NY): Cambridge University Press.

    Google Scholar 

  • Rosenthal SB, Twomey CR, Hartnett AT, Wu HS, Couzin ID. 2015. Revealing the hidden networks of interaction in mobile animal groups allows prediction of complex behavioral contagion. Proc Natl Acad Sci 112(15):4690–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchirico JN, Wilen JE. 2007. Global marine fisheries resources: status and prospects. Int J Glob Environ Issues 7(2–3):106–18.

    Article  Google Scholar 

  • Scheffer M. 2009. Critical transitions in nature and society. Princeton (NJ): Princeton University Press.

    Google Scholar 

  • Scheffer M, Carpenter SR, Lenton TM, Bascompte J, Brock W, Dakos V, Van De Koppel J, Van De Leemput IA, Levin SA, Van Nes EH. 2012. Anticipating critical transitions. Science 338(6105):344–8.

    Article  CAS  PubMed  Google Scholar 

  • Scheffer M, Van Nes EH. 2004. Mechanisms for marine regime shifts: can we use lakes as microcosms for oceans? Prog Oceanogr 60(2):303–19.

    Article  Google Scholar 

  • Sheffer E, Batterman SA, Levin SA, Hedin LO. 2015. Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nat Plants 1:15182.

    Article  CAS  PubMed  Google Scholar 

  • Sherman E, Moore JK, Primeau F, Tanouye D. 2016. Temperature influence on phytoplankton community growth rates. Global Biogeochem Cycles 30(4):550–9.

    Article  CAS  Google Scholar 

  • Shuter B. 1979. A model of physiological adaptation in unicellular algae. J Theor Biol 78(4):519–52.

    Article  CAS  PubMed  Google Scholar 

  • Staver CA, Archibald S, Levin SA. 2011a. The global extent and determinants of savanna and forest as alternative biome states. Science 334(6053):230–2.

    Article  CAS  PubMed  Google Scholar 

  • Staver CA, Archibald S, Levin SA. 2011b. Tree cover in sub-Saharan Africa: rainfall and fire constrain forest and savanna as alternative stable states. Ecology 92(5):1063–72.

    Article  PubMed  Google Scholar 

  • Steele JH. 1998. Regime shifts in marine ecosystems. Ecol Appl 8:S33–6.

    Article  Google Scholar 

  • Strogatz SH. 2014. Nonlinear dynamics and chaos: with applications to physics, biology, chemistry, and engineering. Boulder (CO): Westview Press.

    Google Scholar 

  • Teng YC, Primeau FW, Moore JK, Lomas MW, Martiny AC. 2014. Global-scale variations of the ratios of carbon to phosphorus in exported marine organic matter. Nat Geosci 7(12):895–8.

    Article  CAS  Google Scholar 

  • Toner J, Tu Y. 1995. Long-range order in a two-dimensional dynamical XY model: how birds fly together. Phys Rev Lett 75(23):4326.

    Article  CAS  PubMed  Google Scholar 

  • Toseland ADSJ, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, Lenton TM, Valentin K, Pearson GA, Moulton V. 2013. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Clim Change 3(11):979–84.

    Article  CAS  Google Scholar 

  • Traving SJ, Thygesen UH, Riemann L, Stedmon CA. 2015. A model of extracellular enzymes in free-living microbes: which strategy pays off? Appl Environ Microbiol 81(21):7385–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tunstrøm K, Katz Y, Ioannou CC, Huepe C, Lutz MJ, Couzin ID. 2013. Collective states, multistability and transitional behavior in schooling fish. PLoS Comput Biol 9(2):e1002915.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Turing AM. 1952. The chemical basis of morphogenesis. Philos Trans R Soc Lond B Biol Sci 237(641):37–72.

    Article  Google Scholar 

  • Tyrrell T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400(6744):525–31.

    Article  CAS  Google Scholar 

  • Vallino JJ. 2010. Ecosystem biogeochemistry considered as a distributed metabolic network ordered by maximum entropy production. Philos Trans R Soc Lond B Biol Sci 365(1545):1417–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Cappellen P, Ingall ED. 1994. Benthic phosphorus regeneration, net primary production, and ocean anoxia: a model of the coupled marine biogeochemical cycles of carbon and phosphorus. Paleoceanography 9(5):677–92.

    Article  Google Scholar 

  • Van Nes EH, Scheffer M. 2005. Implications of spatial heterogeneity for catastrophic regime shifts in ecosystems. Ecology 86(7):1797–807.

    Article  Google Scholar 

  • Vetter Y, Deming J, Jumars P, Krieger-Brockett B. 1998. A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb Ecol 36(1):75–92.

    Article  CAS  PubMed  Google Scholar 

  • Vicsek T, Czirók A, Ben-Jacob E, Cohen I, Shochet O. 1995. Novel type of phase transition in a system of self-driven particles. Phys Rev Lett 75(6):1226.

    Article  CAS  PubMed  Google Scholar 

  • Viswanathan GM, Da Luz MG, Raposo EP, Stanley HE. 2011. The physics of foraging: an introduction to random searches and biological encounters. Cambridge (UK): Cambridge University Press.

    Book  Google Scholar 

  • Ward BA, Dutkiewicz S, Jahn O, Follows MJ. 2012. A size-structured food-web model for the global ocean. Limnol Oceanogr 57(6):1877–91.

    Article  Google Scholar 

  • Ward BA, Follows MJ. 2016. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc Natl Acad Sci 113(11):2958–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellington W. 1964. Qualitative changes in populations in unstable environments. Can Entomol 96(1–2):436–51.

    Article  Google Scholar 

  • West SA, El Mouden C, Gardner A. 2011. Sixteen common misconceptions about the evolution of cooperation in humans. Evol Hum Behav 32(4):231–62.

    Article  Google Scholar 

  • Young GF, Scardovi L, Cavagna A, Giardina I, Leonard NE. 2013. Starling flock networks manage uncertainty in consensus at low cost. PLoS Comput Biol 9(1):e1002894.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Simon Levin acknowledges funding from the NSF Dimensions of Biodiversity Grant OCE-1046001, NSF Grant GEO-1211972, NSF Grant OCE-1426746, ARO Grant W911NF-11-1-0385, ARO Grant W911NF-14-1-0431 and by the Nordforsk-funded project Green Growth Based on Marine Resource: Ecological and Socio-Economic Constraints (GreenMAR). George Hagstrom acknowledges funding from NSF Dimensions of Biodiversity Grant OCE-1046001, ARO Grant W911NF-14-1-0431, and ARO Grant W911NF-11-1-0385.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to George I. Hagstrom.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Author's contribution

GIH conceived study, performed research, and wrote the paper. SAL conceived study, performed research, and wrote the paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hagstrom, G.I., Levin, S.A. Marine Ecosystems as Complex Adaptive Systems: Emergent Patterns, Critical Transitions, and Public Goods. Ecosystems 20, 458–476 (2017). https://doi.org/10.1007/s10021-017-0114-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-017-0114-3

Keywords

Navigation