Articles Hsystems umans and their societies depend on natural for a wide range of services that are essential for their well-being. For most of human history, these services have been readily available. It is little surprise, then, that present-day societies tend to take many of these natural services for granted (Daily 1997, Millennium Ecosystem Assessment 2005a, 2006a, 2006b, 2006c, 2006d, 2006e), even while the support systems that provide the services are being severely degraded (Vitousek et al. 1997, Lubchenco 1998). Fish- eries and other resource systems have declined drastically (Pauly et al. 1998, 2002, Myers and Worm 2003, Millennium Ecosystem Assessment 2006f, 2006g, Worm et al. 2006) as a result of overfishing, bycatch, habitat destruction, nutrient and chemical pollution, and selective fishing on apex predators oceans are warming and becoming more acidic (Orr et al. 2005, Royal Society 2005) and novel and reemergent diseases and other invading species have burgeoned as problems (Ward and Lafferty 2004). In the face of these growing challenges to the abilities of human societies to achieve and maintain meaningful and productive lifestyles, we must direct attention to issues of sustainability. For ecosystem services to be sustained over time, the ecosystems providing them must be able to continue functioning in essential ways despite disruptions. In other words, they must be robust and resilient, concepts that have developed somewhat independently in diverse scientific communities to mean much the same thing: the capacity of systems to keep functioning even when disturbed. For the purposes of this article, the central question is this: how do we increase the robustness or resilience of the systems that provide critical ecosystem services, while overcoming the robustness or resilience of systems that yield undesirable phenomena? Given the century-long history of theory on the dynam- ics of ecological systems (going back at least to the work of the great mathematician Vito Volterra) and the practice of managing those systems, we can pose two critical questions: (1) Why has management not been more successful? and (2) Why are we still uncertain about how best to manage crises arising from the magnitude of human impacts on our envi- ronment? The central problem is that both natural and socio - economic systems are complex: they are characterized by multiple possible outcomes and by the potential for rapid change and major regime shifts due to slower and smaller changes in exogenous or endogenous influences (Levin 1999, Simon A. Levin (e-mail: slevin@princeton.edu) is George M. Moffett Professor of Biology and director of the Center for BioComplexity in the Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey. Jane Lubchenco (e-mail: lubchenco@oregonstate.edu) is Wayne and Gladys Valley Professor of Marine Biology and Distinguished Professor of Zoology in the Department of Zoology, Oregon State University, Corvallis. �� 2008 American Institute of Biological Sciences. Resilience, Robustness, and Marine Ecosystem-based Management SIMON A. LEVIN AND JANE LUBCHENCO Marine ecosystems provide essential services to humans, yet these services have been diminished, and their future sustainability endangered, by human patterns of exploitation that threaten system robustness and resilience. Marine ecosystems are complex adaptive systems composed of individual agents that interact with one another to produce collective effects, integrating scales from individual behaviors to the dynamics of whole systems. In such systems, small changes can be magnified through nonlinear interactions, facilitating regime shifts and collapses. Protection of the services these ecosystems provide must therefore maintain the adaptive capacities of these systems by preserving a balance among heterogeneity, modularity, and redundancy, tightening feedback loops to provide incentives for sound stewardship. The challenge for management is to increase incentives to individuals, and tighten reward loops, in ways that will strengthen the robustness and resilience of these systems and preserve their ability to provide ecosystem services for generations to come. Keywords: complex adaptive systems, scale, resilience, robustness, ecosystem management www.biosciencemag.org January 2008 / Vol. 58 No. 1 ��� BioScience 27

Carpenter 2002). Indeed, they are complex adaptive systems in which the dynamics of interactions at small scales perco- late up to shape macroscopic system dynamics, which then feed back to influence the smaller scales (Levin 1998, 2003). It is crucial, then, to understand the linkages among these scales, and to incorporate that knowledge into public aware- ness, management actions, and policy decisions. The vulnerability of marine ecosystems, the value of the ecosystem services they provide, and the need for different ap- proaches in understanding and managing human activities that affect oceans have received much recent attention. Reports from the Pew Oceans Commission (2003), the US Commis- sion on Ocean Policy (2004), the Joint Ocean Commission Ini- tiative (2006), the Millennium Ecosystem Assessment (2006f, 2006g), and Worm and colleagues (2006) draw attention to the seriously disrupted state of marine ecosystems, a result of climate change, coastal development, overexploitation of ocean resources, nutrient and chemical pollution from the land, and other anthropogenic influences. Disruption of ma- rine ecosystems diminishes ecosystem services such as the pro- vision of fish and other seafood, the maintenance of water quality, and the control of pests and pathogens. The collec- tive conclusion of these reports is that if people wish to have safe seafood, stable fisheries, abundant wildlife, clean beaches, and vibrant coastal communities, priority must be given to protecting and restoring the coupled land-ocean systems that provide these services. Both the Joint Ocean Commission and the Pew Oceans Commission conclude that current pub- lic awareness, laws, institutions, and governance practices are insufficient to accomplish these goals. A central recommendation of both commissions is to adopt ecosystem-based management (EBM), reinforcing ear- lier recommendations of the National Research Council (1999). The key challenges are to refine EBM further, and to develop a set of principles to guide management and policy. EBM for the oceans is the application of ecological principles to achieve integrated management of key activities affecting the marine environment. EBM explicitly considers the inter - dependence of all ecosystem components, including species both human and nonhuman, and the environments in which they live. EBM classically defines boundaries for manage- ment on the basis of ecological rather than political criteria, although certainly the political contexts of management must be considered. The goal of marine EBM is to protect, main- tain, and restore ecosystem functioning in order to achieve long-term sustainability of marine ecosystems and the human communities that depend on them (Guerry 2005, McLeod et al. 2005, Rosenberg and McLeod 2005). Marine ecosystems and socioeconomic systems are com- plex adaptive systems. To guide the design and implementa- tion of marine EBM, it will be useful to draw on the knowledge and understanding that are emerging from the exploration of the resilience and robustness of complex adaptive systems. The articles in this special section of BioScience provide guidance about EBM by using the concepts of resilience and robustness as a lens for thinking about complex dynamic systems. Understanding how humans might enhance the robustness and resilience of the systems that provide critical ecosystem services, while thwarting the robustness and resilience of systems that yield undesirable phenomena, will be useful to society. This article summarizes the connections between human well-being and marine ecosystem services, explains why it is useful to think of marine ecosystems as complex adap- tive systems, and describes resilience and robustness as they apply to ocean ecosystems. What do we mean by resilience and robustness? The concepts of robustness and resilience are widely used in the scientific literature, although there is considerable con- fusion about their meanings. The Resilience Alliance (http:// resalliance.org) makes a distinction between engineering resilience (namely, ���the rate at which a system returns to a sin- gle steady or cyclic state following a perturbation���) and eco- logical resilience (namely, ���the amount of change or disruption that is required to transform a system from being main- tained by one set of mutually reinforcing processes and struc- tures to a different set of processes and structures���). The latter definition, which reflects the focus of the Resilience Alliance, seems closest to that introduced by Holling (1973) in his seminal paper but it is clear that the notion of resilience is sometimes interpreted in the general literature in the nar- rower sense of recovery from disturbance, and at other times in the broader sense of the maintenance of functioning in the face of disturbance. Within this article, we adopt the broader definition, and we do not distinguish it from robustness. Parallel ideas have developed in other scientific commu- nities. In materials science, two concepts are central: stress, or the force tensor applied to a system, and strain, or the defor- mation tensor that results from the application of the stress. These concepts have relevance for ecological systems as well, and failure to distinguish between stress and strain can lead to confusion. In the face of stressors, whether endogenous or exogenous, both the ability to resist deformation (strain) and the ability to recover from deformation are important. That is, it is important to recognize that there are two key aspects of what may be called robustness (or resilience): (1) resistance to change (as well as flexibility, the amount a system can be perturbed from its reference state without that change being essentially irreversible) and more generally, (2) the ability of the system to recover. Such a definition is also concordant with what in developmental biology is termed developmental robustness���namely, ���the capacity to stay ���on track��� despite the myriad vicissitudes that inevitably plague a developing organism��� (Fox Keller 2002). In turbulent marine systems, for example, organisms may weather the waves (thereby achieving robustness) either by resisting fluid dynamical stresses with a rigid structure, as barnacles or corals do, or by going with the flow, as the flexible large kelp do. Considering these multiple aspects of robustness and resilience requires attention to the related concepts of resis- tance, recovery, and irreversibility, as developed in the article by Palumbi and colleagues (2008). Articles 28 BioScience ��� January 2008 / Vol. 58 No. 1 www.biosciencemag.org