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Confronting Feedbacks of DegradedMarine Ecosystems

Magnus Nystrom,1* Albert V. Norstrom,1 Thorsten Blenckner,1,2 Maricelade la Torre-Castro,1,3 Johan S. Eklof,3,4 Carl Folke,1,5 Henrik Osterblom,1,2

Robert S. Steneck,6 Matilda Thyresson,1,3 and Max Troell1,5

1Stockholm Resilience Centre, Stockholm University, Stockholm, Sweden; 2Baltic Nest Institute, Stockholm Resilience Centre,Stockholm University, Stockholm, Sweden; 3Department of Systems Ecology, Stockholm University, Stockholm, Sweden;

4Department of Biology and Environmental Sciences, Goteborg University, Goteborg, Sweden; 5The Beijer Institute,The Royal Swedish Academy of Sciences, Stockholm, Sweden; 6School of Marine Sciences, University of Maine,

Darling Marine Center, Walpole, Maine, USA

ABSTRACT

In many coastal areas, marine ecosystems haveshifted into contrasting states having reduced eco-system services (hereafter called degraded). Suchdegraded ecosystems may be slow to revert to theiroriginal state due to new ecological feedbacks thatreinforce the degraded state. A better understand-ing of the way human actions influence thestrength and direction of feedbacks, how differentfeedbacks could interact, and at what scales theyoperate, may be necessary in some cases for suc-cessful management of marine ecosystems. Herewe synthesize interactions of critical feedbacks ofthe degraded states from six globally distinct bio-mes: coral reefs, kelp forests, seagrass beds, shallowsoft sediments, oyster reefs, and coastal pelagic food

webs. We explore to what extent current man-agement captures these feedbacks and proposestrategies for how and when (that is, windows ofopportunity) to influence feedbacks in ways tobreak the resilience of the degraded ecosystemstates. We conclude by proposing some challengesfor future research that could improve our under-standing of these issues and emphasize that man-agement of degraded marine states will require abroad social–ecological approach to succeed.

Key words: alternative states; degradation; feed-backs; management; marine ecosystems; regimeshift; resilience; restoration.

INTRODUCTION

Ecosystems can rapidly change to a contrasting state.When the dominant organisms for which the eco-system was described become rare, or when the

ecosystem services as perceived by people declinesignificantly, we call this alternative ecosystem state‘‘degraded.’’ Patterns of change from one ecosystemstate to another (such as a regime shift) tell usnothing per se about rate of recovery to the initialstate. Regime shifts and phase shifts can revertimmediately back to their initial states (for example,Steele 1998; Done 1992, respectively). However, lagsin recovery (also called ‘‘hysteresis’’ sensu Schefferand others 2001) can be protracted and in some casesresult in ecosystems becoming locked into degradedconditions, which can be described as being in analternative stable state (Petraitis and others 2009).

Received 25 August 2011; accepted 19 February 2012

Author contributions: The original idea was developed by MN and AN.

MN and AN wrote the first draft of the manuscript, all authors contrib-

uted to specific sections (coral reefs: MN, AN, M. Thyresson, RSS; kelp:

RSS; seagrass beds: JSE, MdlTC; naturally unvegetated shallow-bottom

habitats: M. Troell; oyster beds: MN, M. Troell, AN; coastal pelagic food

webs: HO, TB) and all authors contributed to general text development.

*Corresponding author; e-mail: magnus.nystrom@stockholmresilience.su.se

EcosystemsDOI: 10.1007/s10021-012-9530-6

! 2012 Springer Science+Business Media, LLC

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Although examples of alternative stable statesexist in the literature (Scheffer and Carpenter2003), debate continues about how they should bedefined and what constitutes proof of their exis-tence (Petraitis and Dudgeon 2004; Petraitis andothers 2009). The most clearly articulated criteriaindicate that changes must occur at the exact samesite, result in different communities that are capa-ble of self-replication for more than the generationfor the dominant organism and be the result of apulse (not ‘‘press’’) perturbation (Petraitis andothers 2009). Empirical evidence of these alterna-tive states determined that they were triggered bychanging ‘‘external’’ environmental conditions(Scheffer and Carpenter 2003). However, mostempirical examples illustrated small-scale, oftenlaboratory controlled, experiments (Schroder andothers 2005) thus there remains the challenge ofscaling up this class of interaction to spatially sig-nificant ecosystems (Bertness and Leonard 1997;Scheffer and others 2001). Nevertheless, theabsence of strong proofs of alternative stable statesfrom field data does not imply that they do not exist(Scheffer and Carpenter 2003). There are ampleexamples from lakes and grasslands and otherbiomes (Scheffer and others 1993; Carpenter andothers 2011; van de Koppel and others 1997).Intuitively, it seems reasonable that alternativestable states may also exist in other ecosystems(van Nes and Scheffer 2004).Accumulated experience from coral reefs

(Hughes 1994; Mumby and others 2007), kelpforests (Steneck and others 2002), seagrass beds(van der Heide and others 2007), coastal pelagicecosystems (Beaugrand 2004; Mollmann and oth-ers 2009), oyster reefs (Schulte and others 2009),and other systems (for example, blue mussel beds,Mytilus edulis) (Petraitis and others 2009), suggestthat marine ecosystems can undergo rapid changeto a contrasting state where they may remain for aprotracted period. This locking of ecosystems in adegraded state is the bane of managers and policymakers. Witness, for example, failed attempts torestore Atlantic cod dominance in the westernNorth Atlantic despite large no-take regions(Hutchings and Reynolds 2004) or other attemptsto reverse coastal eutrophication (Duarte and oth-ers 2009). In those cases, as with all that involveecosystem hysteresis, simply reducing drivers orconditions back to values prior to the flip, has notresulted in recovery. The focus of our paper is tobetter understand the conditions that preventrecovery of such complex nature systems. Wesuggest that in many cases driving ecological pro-cesses change when the ecosystem degrades and

these can affect other processes in a way that canlock the system into its alternative state. Morespecifically, we suggest that new ecological feed-backs can become established that reinforce thechanged state.

Here we review strong ecological feedbacks thatcould contribute to reinforcing degraded states ofmarine ecosystems. Then we suggest how humanscan affect such feedbacks, at what scale thesechanges manifest and how different feedbacksinteract with one another. For this purpose, wedraw on examples from six of the world’s majorshallow water biomes: coral reefs, kelp forests,seagrass beds, naturally unvegetated shallow-ben-thic habitats, oyster reefs, and coastal pelagic foodwebs. The mere presence of feedback loops doesnot necessarily indicate they will lock the ecosys-tem into an alternative (Schroder and others 2005)and the aim here is not to evaluate evidence for oragainst whether these degraded marine states rep-resent true alternative stable states, but to synthe-size what we have learned about feedbacks thatcould create obstacles for managers whose missionis to reverse degraded marine ecosystems. For eachecosystem, we explore how current managementapproaches are geared to break unwanted feed-backs and briefly discuss how certain events couldact as catalysts that facilitate this process (that is,windows of opportunity). We conclude by pro-posing some challenges for future research thatcould improve our understanding of these issues.We begin by recapitulating how ecological feed-backs can influence the behavior of ecosystems.

ECOLOGICAL FEEDBACKS

Negative (‘‘dampening’’ or ‘‘stabilizing’’) and po-sitive (‘‘amplifying’’ or destabilizing) feedbacks arean integral part of all natural systems and involvebiological, physical, and chemical processes. Nega-tive feedbacks tend to reduce fluctuations, createattractors, and stabilize key drivers (that is, keepingthe system within a particular state), whereas po-sitive feedbacks amplify changes in processes thatdestabilize the system. Pulse perturbation (forexample, storms, hurricanes, disease outbreaks) orpress perturbations (for example, loss of habitat,fishing pressure eutrophication, elevated tempera-ture) can overwhelm negative feedbacks makingpositive feedbacks dominant. If these positivefeedbacks are strong enough in relation to otherecosystem processes, they can drive the systemacross a threshold and into an alternative state,characterized by a new set of negative feedbacks,which could provide some degree of stability to the

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new possibly degraded state (Scheffer and others2001). However, the feedback terminology is di-verse, and sometimes contradictory. For the pur-pose of this review, we will focus on feedbacks thatpush marine ecosystems away from (destabilize), orreinforce (stabilize) contrasting states.Unstable co-existence between species can gen-

erate simple but effective biotic feedbacks. Forexample, if inter-specific competition is strong thenchanges in the relative abundance of a dominantspecies (for example, mass mortality) can beamplified through a range of mechanisms exertedby another species, such as recruitment preemp-tion, overgrowth, and allelophathy (for example,Mumby and Steneck 2009, Rasher and Hay 2010).This dominance can be further reinforced by den-sity-dependent processes, such as low fertilizationsuccess (that is, Allee effect) (see ‘‘Coral reefs’’section) and competitive ability (that is, whenspecies exert stronger competition effects in groupsthan as individuals). Biotic feedback loops can alsoemerge among species interacting across trophiclevels in situations when simple interaction hier-archies are absent. Intuitive examples are situationswhere temporary reductions in predation allowprey to grow in size and escape predation (size-selective predation) (Mumby and others 2006),where prey species can control predator abun-dances by feeding on their predators’ juveniles(prey-to-predator loops) (Bakun and Weeks 2006)(see ‘‘Coastal pelagic food webs’’ section), or whena top-down regulator changes its behavior as aresponse to changes in the abundance of the speciesit controls (that is, functional response, Hoey andBellwood 2011) (see ‘‘Coral reefs’’ section).Feedbacks driven by biotic–abiotic interactions

have been suggested as a key element in the trig-gering of switches between alternative (stable)states (Scheffer and others 2001). For example, thepresence of vegetation in dry terrestrial ecosystemscan improve soil moisture, soil insulation, soil sta-bility, and provide protected shade for seedlings.This leads to a feedback loop where vegetationenhances growth and reinforces a vegetated state.If these feedbacks are reversed, an increasinglyharsh environment for plants can ultimately lead toa stable vegetation-free (degraded) state (van deKoppel and others 1997). However, sometimesthere is a mixed situation where biotic feedbacksand biotic–abiotic interactions in a system acttogether. For example, in shallow lakes, submergedplants compete with phytoplankton by altering the(abiotic) light and nutrient conditions by capturingsediment particles in the water column and hamperresuspension of sediment. This stimulates further

growth of plants and reinforces a vegetated clear-water state. If turbidity suddenly increases (forexample, an input of nutrients that generatesextensive phytoplankton blooms), benthic vegeta-tion will disappear once a critical point of turbidityis reached. Loss of vegetation reduces sedimentstabilization, which increases turbidity even furtherand the lake may eventually shift to a turbid waterstate (Scheffer and others 1993). This feedbackcauses the turbid state to be a self-stabilizingalternative to the clear situation. Similarly, bivalve-beds may provide physical stability while at thesame time reducing anoxia risks by loweringorganic matter production through their grazing onphytoplankton (Schulte and others 2009) (see‘‘Oyster reefs’’ section).

Breaking Feedbacks

Breaking feedbacks primarily driven by bioticinteractions typically requires suppressing pro-cesses that control ‘‘undesirable’’ species, and/orrestoring processes necessary for desirable speciessuch as reversing trophic structures and historicbiotic disturbances (for example, grazing) (Sudingand others 2004). Breaking biotic–abiotic feedbacksis often more complicated because abiotic changescan profoundly alter site characteristics (for exam-ple, soil salinization, eutrophication, soil nutrientcontent, habitat). In some cases, ‘‘resetting’’ adriving process or processes may be sufficient tobreak feedbacks and instigate a shift of an entireecosystem. In the Danish historically nutrient-stressed Ringkobing Fjord, a small change insalinity, by a change in sluice management, facili-tated new recruitment of the suspension-feedingsoft-shell clam Mya arenaria (Petersen and others2008). By clearing the water column from pelagicalgae, the mussels caused a rapid system shift froma bottom-up controlled turbid state, to a top-downcontrolled clear-water state. In other situations,management approaches might need to consider abroader set of factors that operate at multiple scales(Suding and others 2004). Such strategies have beeneffective in restoration of shallow lakes wherebiomanipulation through a sudden reduction of fishbiomass (pulse-overfishing) can, in conjunction withreduced levels of nutrients, break the feedbacks of aturbid state and shift the lake back to a clear-waterstate (Søndergaard and others 1990). Importantly,management needs to be aligned with the scales atwhich critical feedbacks operate (see ‘‘Oyster reefs’’section).

Although feedbacks have been recognized as animportant part of the dynamics and behavior of

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marine ecosystems their interactions and ways tobreak them are poorly understood. Below wereview critical feedbacks of the degraded states insix major biomes, and explore to what extentcontemporary management capture these.

FEEDBACKS IN DEGRADED MARINE

ECOSYSTEM STATES

Coral Reefs

Worldwide loss of coral reefs (Gardner and others2003; Bruno and Selig 2007), owing to humanimpacts, is repeatedly associated with shifts fromcoral to macroalgal dominance, although otherpotential alternative states have been suggested(Norstrom and others 2009). A suite of feedbackshas been proposed to strengthen the dominance ofmacroalgae on a reef once they become abundant(Mumby and Steneck 2008) (Figure 1A). Algaepreempt space and increase sediment retentionreducing coral growth and preventing settlement ofcoral larvae (Birrell and others 2005). They alsopromote coral mortality through toxicity (Rasher

and Hay 2010), disease transmission and enhancedmicrobial activity (Smith and others 2006) andovergrow juvenile and low relief adult coral colo-nies (Box and Mumby 2007). Such local feedbackscan be augmented by direct human impacts such asoverexploitation of algal consumers (for example,herbivorous fish and sea urchins) and severe pulsedisturbances (for example, hurricanes, coral dis-eases, coral bleaching event) that kill corals andliberate colonizing space for opportunistic algae.When this happens, proportionally fewer herbi-vores graze per area of algal-covered reef, hence,increasing the likelihood for macroalgae to even-tually proliferate on the freed substratum (Mumbyand others 2007). Unless recruiting macroalgae aregrazed and kept as low-canopy turf, they can reacha size at which they become unpalatable to mostherbivorous fish (Bellwood and others 2006).Experimental manipulation of macroalgal (Sargassum)density also suggests that herbivorous fish mightavoid dense macroalgal patches, possibly as a gen-eral aversion to a habitat in which predators arelikely to be found (Hoey and Bellwood 2011).If this foraging behavior holds true for reefs in

A B

Figure 1. A schematic illustration of reinforcing feedbacks in degraded coral reefs. Human impacts and natural pulsedisturbance can generate a range of feedbacks that emerge through the outcomes of local competitive interactionsbetween corals and macroalgae (A). Undesirable macroalgal states on coral reefs are maintained by multiple feedbackloops that can interact over spatial and temporal scales (B). Feedbacks generated by local competitive interactions betweencorals and macroalgae (1) are strengthened over time when declines in the numerical abundance and biomass of her-bivorous organisms, due to a loss of habitat complexity on the reef, further restrain the control of macroalgae (2). As thenumber of degraded reefs increases, coral broodstocks are lost and connectivity between coral-dominated reefs is reduced,potentially leading to recruitment failure and regional reproductive Allee effects (3).

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general it illustrates a previously unknown feed-back mechanism that could reinforce algal-domi-nated states.At an intermediate time-scale (5–10 years) coral

mortality can lead to a reduction in habitat com-plexity (Alvarez-Filip and others 2009) and sub-sequent loss of recruitment habitats for key reeffish including herbivores (Jones and others 2004;Lee 2006). Other declines in the numerical abun-dance and biomass of herbivorous fish (Grahamand others 2007) may, in combination withoverfishing, liberation of large tracts of substratum,and local biotic feedbacks, send reefs into a spiral ofdegradation (Figure 1B).If an increasing number of reefs within the sea-

scape shift to algal dominance, broader-scale feed-backs may come into play and reinforce thoseoperating at more local scales (Elmhirst and others2009) (Figure 1B). For example, the reproductivesuccess of sexually reproducing reef organisms maydepend on a critical broodstock size or populationdensity, below which the population declines dueto low fertilization success, a so-called Allee effect(Gascoigne and Lipcius 2004). Regional recruit-ment failure of corals and invertebrate herbivoresin response to the crossing of such thresholds canprevent regeneration of locally deteriorated coralreefs (Knowlton 1992; Nystrom and others 2008).

Breaking Feedbacks in Degraded Coral Reefs

Manual clearing of macroalgae has been proposedas a potential strategy to break biotic feedbacks (forexample, space preemption, overgrowth, andunpalatable life-stages of macroalgae) betweencorals and algae, and open up space for coral larvalrecruitment (McClanahan and others 2001).Although being too time consuming and costineffective to implement at large spatial scales, itmay offer a strategy for small areas of particularinterest, such as conservation sites and populardiving locations. Preconditioning reefs by imple-menting temporary fishing restrictions to increasethe abundance of herbivorous fish before removalschemes are initiated may increase the likelihoodthat algal establishment and growth will be kept incheck. When sea urchins (Diadema antillarum)returned on some reefs in the Caribbean, a corre-sponding decrease in macroalgal abundance andincrease in coral abundance was observed (Car-penter and Edmunds 2006). This gives some weightto the suggestion that artificial enhancement of keyprocesses, such as herbivory from sea urchins(Macia and others 2007) or grazing fish (Conklinand Stimson 2004; Mumby and Steneck 2008),

could be a potential tool to reduce algae on reefsand help key herbivores overcome recruitmentfailure allowing grazing to be naturally maintainedin the long-term. However, this strategy has tobecome more cost-effective to be a useful approachat large scale.

No-take fishing reserves have been suggested as ameasure to improve ecosystem structure and trophicinteractions (for example, Hughes and others 2005).For example, Mumby and others (2006) demon-strate that biomass of herbivorous parrotfish washigher inside a well-managed reserve than outside,and that parrotfish biomass and cover of macroalgaewas negatively correlated. However, increased bio-mass of herbivorous fish may not be sufficient toreverse algal-dominated states if the wider seascapehas been degraded and coral propagules are a limit-ing factor (Hughes and others 2010).

Active coral transplantation has been promotedas a tool to restore heavily impacted or denudedcoral reefs where the prospects for natural recoveryare extremely low (for example, lack of coralbroodstocks). The outcomes are small and costs arehigh of these transplantation programs. None havebeen shown to succeed at an ecologically mean-ingful scale (for example, an entire coral reef). Thisraises questions about the ecological and economiccosts associated with the collection (for example,impacts in the donor areas), rearing, and trans-plantation of individuals (Adger and others 2005).

Kelp Forests

Kelp forests create the largest biogenic structures inthe sea. Kelp canopies reduce the light reaching thebenthos (Gerard 1984) and can impede the larvalsupply of shore-dwelling invertebrates (Gaines andRoughgarden 1987). Similarly, kelp and other al-gae house hundreds of species that depend on algalhabitats for shelter and food (Hacker and Steneck1990; Christie and others 2009). Therefore, kelpdeforestation creates significant collateral damageto the ecosystem and affects myriad of associatedorganisms. Some organisms associated with kelp-forest ecosystems can be strong interactors (sensuPaine 1992; Sala and Graham 2002) that drive thedistribution and abundance of other organisms andthus define the structure and functioning of theecosystem. Globally, the strongest driver of kelpdeforestation is grazing sea urchins (Steneck andothers 2002) and feedbacks controlling them alsocontrol kelp-forest stability.

In the western North Atlantic, impacts ofsequential fishing have generated coastal trophiccascades. Specifically, overfishing of large

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predatory fishes such as Atlantic cod resulted inpopulation explosions of species such as lobsters,crabs, and sea urchins that formerly had been prey(Steneck 1997; Steneck and others 2004). Seaurchins were an important beneficiary of predatorrelease and, being the only significant herbivore inthis ecosystem, their increase resulted in completedeforestation and dominance by herbivore-resis-tant calcareous coralline algae. The system lockedinto what is known as a ‘‘sea urchin barrenground’’ because the absence of erect algae givespredators capable of eating settling sea urchin lar-vae nowhere to hide (Figure 2). As a result, fre-quent sea urchin recruitment locks the benthosinto a persistent algal-free state (Sivertsen 1997). InMaine, on the northeast coast of the US, this wouldhave persisted indefinitely had a fishery for seaurchin roe (gonads) not developed. The sea urchinfishery began in 1987, peaked in 1993, and had

largely collapsed due to overfishing by 2000(Steneck and others 2002, 2004) (Figure 2). Thefisheries-induced declines of sea urchins demon-strably reduced herbivory thereby driving a shiftback to kelp-dominance (Steneck 1997). Becausethe resulting algae created refugia for recruiting crabmicropredators that eat settling sea urchins, andbecause no apex predators could limit crab popula-tions, recruitment of sea urchins effectively halted(Steneck and others 2002) (Figure 2). In both cases,human activities create reinforcing feedbacks byindirectly changing the recruitment potential of thebenthos making it initially more receptive and thenless receptive to settling sea urchins.

Breaking Feedbacks in Degraded Kelp Ecosystems

Shallow marine ecosystems, with less mobile orsedentary species, might lend themselves to

Figure 2. The top panel illustrates temporal trends in the relative abundance of groundfish (solid), sea urchins (dotted) andkelp (line-dot-line) in Maine (northeast coast of the US) between the 1930s and present date (adopted from Steneck andothers 2002). The fisheries-induced decline of groundfish resulted in trophic cascades in which sea urchins becameincreasingly abundant until their demise around 1993 as a consequence of overharvesting. Following the sea urchindecline previously suppressed kelp and smaller canopy algae were able to return. The bottom figure depicts the fisheries rolein mediating kelp-dominated and sea urchin barren grounds, and the feedbacks involved in maintaining these states.CCA is acronym for calcareous coralline algae, which hamper kelp recruitment and stimulate settlement of sea urchins.

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targeted removals to break biotic feedbacks. The seaurchin fishery in Maine illustrates how an unex-pected human-induced shock (the development ofa sea urchin fishery) was able to halt overgrazingcaused by hyperabundant sea urchins, therebyallowing kelp to return (Figure 2). Although thishuman intervention was not driven by a purpose-ful management action, but by a market demandfor sea urchin roe, it shows that critical feedbackscan be broken in marine ecosystems through tar-geted removals. It also suggests that commercialinterests could (if controlled and managed adap-tively) be aligned with management goals by cre-ating incentives for fishing of species underpinningproblematic feedbacks.

Seagrass Beds

Seagrasses create a self-facilitating environment byreducing levels of nutrients in the water column,attenuating water flow, and stabilizing sedimentsthat reduce water turbidity, thereby improving lightpenetration and seagrass growth conditions (van derHeide and others 2007). However, seagrass beds aredisappearing at an accelerating rate globally due to a

broad spectrum of anthropogenic and natural causes(Waycott and others 2009). This is of great concernbecause of the potential bi-directional influence offeedbacks, which may lead to undesirable alterna-tive states that are resilient to restorative efforts(Figure 3). An illustrative example is the DutchWadden Sea (van der Heide and others 2007) wherepreviously eelgrass-dominated beds (Zostera marina),shifted to a bare sediment state in the early 1930s.The shift was initially caused by a combination ofthe 1930s ‘‘wasting disease,’’ a protist infection thatkilled as much as 90% of all eelgrass in the NorthAtlantic Ocean, and eutrophication. In a model, vander Heide and others (2007) suggest altered hydro-dynamics as a major driver for the observed lack ofrecovery: when seagrass cover was high, roots andrhizomes stabilized sediment and their leaves trap-ped floating particles and attenuated water flow,reducing turbidity, and promoting seagrass growth.As seagrass cover decreased below a threshold,current and wave velocities increased and sedimentstabilization was lost. This resulted in increasedturbidity, reduced growth and density of remainingseagrasses, and prevented seagrass recruits fromestablishing (Figure 3). Loss of seagrass can also lead

Figure 3. A schematic illustration of reinforcing feedback loops in two degraded states of seagrass beds. The bare sedimentstate (left loop) is reinforced by sediment instability (due to loss of seagrass, their roots and rhizomes) causing burial,increased turbidity and reduced light irradiance, which hampers growth and recruitment of seagrass. Input of nutrientsand reduced top-down control (that is, grazing) can generate a filamentous algal-dominated state (right loop) leading toovergrowth of seagrass and/or formation of dense algal mats and anoxia that suffocate the seagrass.

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to an accumulation of toxic sediment sulfide(because of reduced seagrass oxygenation of sedi-ments), which in turn has been shown to increaseroot and rhizome mortality (Azzoni and others2001).In sheltered near shore areas, seagrass beds can

become dominated by ephemeral micro- and mac-roalgae (Duarte 1995). This shift is typically drivenby a combination of eutrophication and reducedgrazing pressure on algae. Once the algae are inplace, a set of feedbacks can reinforce their presence(Figure 3). For example, nutrients released fromdecaying plant detritus and sediment can stimulatenew algal growth, and increasing respiration tobreak down the excess detritus causes bottomanoxia, which hampers grazer survival (Duarte1995). In the Greifswalder Bodden estuary (SWBaltic Sea), attempts to facilitate seagrass recoloni-zation by reducing nutrient inputs from land-basedsources failed, because sediment-bound phospho-rous continues to stimulate phytoplankton blooms(Munkes 2005).

Breaking Feedbacks in Degraded Seagrass Beds

Loss of seagrass beds has triggered numeroustransplantation programs, but the costs are highand success rates are low (Orth and others 2006).Seagrass transplantation operations are typicallyattempted at small (<1 ha) scales, which mayexplain their low score of accomplishment. Becausesediment instability and high turbidity can severelyhamper the survival of seagrass transplants trans-plantation operations should be executed at scaleslarge enough to overwhelm scale-dependent bio-tic–abiotic feedbacks, such as sediment destabiliza-tion, to instigate self-facilitation (van der Heide andothers 2007; van Katwijk and others 2009). Ifaccompanied by supplementary measures, such asinvestments in mussel beds that create beneficialshelter for seagrass transplants, the self-facilitativeproperties of seagrass could be enhanced (vanKatwijk and others 2009).Restoration of distorted food webs in seagrass

beds has been proposed as a way to break rein-forcing feedbacks in micro-/macroalgal-dominatedstates. Munkes (2005) suggests that re-stocking oflarge predatory fish (for example, gadoids) couldreduce densities of mesopredators (for example,small predatory fish, crabs, and shrimp) that sup-press algal mesograzers (for example, crustaceans,gastropods) controlling micro-/macroalgae. Thisstrategy could potentially be aligned with a con-tinual manual removal of filamentous macroalgaeto reduce a major pool of nutrients from the system

that potentially ameliorates the risk for physicalovergrowth of recovering seagrass.

Shallow Naturally UnvegetatedSoft-Bottom Habitats

In many temperate regions soft sediment habitats,naturally characterized by sparse or very patchymacrovegetation, constitute a substantial propor-tion of the shallow (0–1 m depth) coastal zone.Unlike the alternative degraded unvegetated statein seagrass beds, these habitats are characterized bya substantial production of microphytobenthicalgae (Sundback and others 2003) and are impor-tant nursery and feeding grounds for many fishspecies (Gibson 1994; Pihl and Wennhage 2002).

In many parts of the world previously pristineestuaries and coastal waters are increasingly suf-fering extensive macroalgal blooms (Valiela andothers 1997). Shallow areas along the Swedishwest coast, for example, have experienced shifts tostates characterized by ephemeral macroalgalblooms (Osterling and Pihl 2001); dense green algalmats (belonging to the genera Cladophora andEnteromorpha) can cover 30–50% of the total shal-low soft-bottom habitat in the Swedish SkagerrakCoast archipelago during summer (Pihl and others1999). Increased nutrient loading to coastal watersand coastal sediments has been proposed as themain driver (Sundback and others 2003; Troell andothers 2005), but reduction of grazers (causingchanges in trophic interactions as documented inseagrass beds, Baden and others 2010) and oxygendeficiency (Engelsen and Pihl 2008) may also playimportant roles. The new state seems persistentagainst management efforts, such as reduction ofnutrient run-off from land and harvest of the algae(Sundback and others 2003), due to a set of feed-back mechanisms that reinforce the algal domi-nance. Similar to the feedbacks operating indegraded seagrass systems (Figure 3), increaseddensities of filamentous algae precipitate anoxicconditions through increased algal respirationrates, decreased water circulation, and increasedaccumulation and decomposition of dead algalmatter, causing nutrients to accumulate in thesediment that stimulates further algal growth(Norkko and Bonsdorff 1996; Sundback and others2003). Moreover, shading caused by algal mats andthe preemption of microphytobenthic organismsettlement space may cause decreased oxygenation,bioturbation, and grazing activity, thus facilitatingfurther accumulation of nutrients in the sedimentpool (Troell and others 2005; Engelsen and Pihl2008). Macroalgal blooms are seasonal events in

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the temperate zone, and over-wintering spores andother propagules promote rapid re-development asenvironmental conditions improve during summer.Accumulation of algal propagules in the sediment,associated with proliferating summer blooms, canthus create ‘‘dormant’’ feedback processes thattemporally could reinforce this state.

Breaking Feedbacks in Degraded UnvegetatedSoft-Bottom Habitats

Attempts to reverse the degraded state by reducingnutrient inputs (from direct and indirect sources)and manually removing filamentous algae have sofar proven unsuccessful. This highlights theimportance of feedbacks structured around sedi-ment-bound nutrients in reinforcing the degradedalgal state. Reduced fishing pressure could poten-tially change trophic structures leading to anincreased grazing rate. A more radical strategy tobreak out of these states could be to take away thetop-layer of sediment to remove accumulatednutrients and algal spores. This, however, seemsunattainable considering the scale of affectedcoastal areas. For estuaries experiencing problemswith macroalgae blooms, it has been suggested thatimproving hydrological conditions, that is, lower-ing the water residence time of the system, canreduce macroalgal growth (Lillebø and others2005).

Oyster Reefs

Estuarine oyster reefs worldwide have suffered greatdeclines owing to overfishing, habitat destruction,invasive species and diseases (Jackson and others2001; Kirby 2004; Lotze and others 2006). Economicand ecological losses involve oyster production, hab-itat formation, biodiversity, and trophic complexity(Coen and others 2007; Schulte and others 2009).Oysters are ‘‘ecosystem engineers’’ in the sense

that they can have a significant impact on theirabiotic surrounding environment. One importantfunction is limiting/controlling phytoplanktonblooms through grazing. Being suspension-feeders,oysters also remove organic material from thewater column and thereby divert production fromthe water column to the benthos. It has been sug-gested that the demise of oyster reefs in manyestuaries is a key driver behind the observedeutrophication and subsequent hypoxia/anoxiadue to increased microbial decomposition (Jacksonand others 2001), although the potential benefits offiltration has been questioned (Pomeroy and others2006). Oysters (live and dead) also serve as criticalsubstratum for oyster sprat settlement, and provide

stabilization of benthic and intertidal habitats. Ifoysters are lost (that is, loss of sediment stabiliza-tion), the sediment deposition rate can increase,which may suffocate existing oysters and preventsettlement of new recruits. Furthermore, increasedsediment in the water column also increases theenergy expenditure for oysters to filter the water,thereby increasing susceptibility to disease andmortality rates (Lenihan and others 1999).Together these factors may eventually push oysterreefs into an alternative degraded oyster-free sedi-ment-dominated state, which is reinforced by sed-iment instability, phytoplankton blooms, andhypoxia/anoxia (Schulte and others 2009). Indeed,bifurcation analysis and numerical simulationssuggest that multiple stable equilibria exist, onestate with oysters and an oyster-free state (Jordan-Cooley and others 2011).

Breaking Feedbacks in Degraded Oyster Reefs

The valuable oyster fishery has, along with otherreef-associated ecosystem services resulted in a broadappeal for restoration of oyster reefs (Coen and oth-ers 2007). But these efforts have been unsuccessfuldue to, for example, continuous (destructive) har-vesting; loss of broodstocks, low recruitment, lowhabitat quality, and/or the inability of introducednon-native oyster species to cope with diseases(Lotze and others 2006). However, in a field exper-iment, Schulte and others (2009) demonstrated howa highly resilient, sediment-dominated oyster reef inChesapeake Bay (a sub-estuary in eastern US) couldbe successfully reversed through a spatially extensive(35 ha) habitat restoration, in combination with aban on oyster harvesting. By providing high verticalrelief habitats, oysters were allowed to escape sedi-ments and hypoxia. This promoted growth of oystersand triggered a reinforcing feedback between adultdensity and subsequent juvenile recruitment thatoverwhelmed the previous recruitment bottleneck.The study illustrates how restoration, if carried out atappropriate scales can break feedbacks that maintainoyster reefs in a degraded sediment state and bolsterprocesses that reinforce oyster reef accumulation.

Coastal Pelagic Food Webs

Dramatic shifts in coastal pelagic ecosystems havebeen reported throughout the world (Figure 4A, B)and are often described as climate-induced and/orfisheries-related collapses leading to alternativestates dominated by species at lower trophic levels(Collie and others 2004; Lees and others 2006).A range of feedbacks and their interactions can pre-vent recovery of collapsed fish stocks (Figure 4C),

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A

B

C

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and hence the reversal of economically undesirablestates. For example, overharvesting of predatoryfish alters trophic relationships and competitiveinteractions which can lead to prey to predatorfeedback loops (Bakun 2006). Such trophic chan-ges have been suggested to underlie the recoveryfailure of collapsed cod stocks (Gadus morhua) in theBaltic Sea and North Atlantic, where high densitiesof sprat (Sprattus sprattus) and herring (Clupeaharengus) hamper cod recruitment by feeding onthe eggs and larvae of their predators (Koster andMollmann 2000) or compete with cod larvae forzooplankton prey (Casini and others 2009). Similarmechanisms have also been proposed to underpinjellyfish-dominated states where copious jellyfishpopulations, associated with overexploitation ofsmall planktivorous fish (anchovy or sardine),exert a top-down control on fish eggs and larvae(Daskalov and others 2007; Richardson and others2009). As the jellyfish become more abundant,their recruitment output increases (as the likeli-hood for successful fertilization increases) andsurrounding overfished areas may become infested,generating blooms and feedbacks at even largerspatial scales (Richardson and others 2009). Theseinteracting self-reinforcing feedback loops (Fig-ure 4C) can contribute to increase the stability ofjellyfish-dominated states, which may generatedurable shifts that are difficult to revert throughsingle management actions.Prey-to-predator loops can also be reinforced by

feedbacks related to climate and the biogeochemi-cal state of fish spawning areas (Figure 4C). In theBaltic Sea, successful cod spawning depends onsufficient levels of deep-water oxygen. This is in

turn influenced by the inflow of highly oxygenatedand saline water from the North Sea, nutrientinputs, and primary production levels (Mollmannand others 2009). Increased primary productionand the accumulation of a phosphorus pool in thedeep basins of the Baltic Sea may have caused abiogeochemical regime shift from oligotrophic toeutrophic conditions (Osterblom and others 2007).This new biogeochemical state seems to be stabi-lized by a feedback where phosphorus releasedfrom the sediment in response to eutrophic condi-tions, stimulates the growth of N-fixing cyanobac-teria. Cyanobacterial decomposition may promotefurther increases in oxygen consumption and therelease of phosphorus from the sediment (Conleyand others 2002). It has also been suggested thatreductions of predatory fish stocks may changetrophic structures leading to increased summerphytoplankton production (Frank and others 2005;Daskalov and others 2007). An increase in summerphytoplankton production (and thus deep-wateroxygen demand, at least in the Baltic Sea) canfurther strengthen the feedbacks between deprivedenvironmental conditions (anoxia) and overfish-ing.

Breaking Feedbacks in Degraded Pelagic Coastal FoodWebs

Prey-to-predator feedback loops in coastal pelagicsystems could potentially be arrested throughmanagement trials where populations of smallpelagic forage fish are deliberately overfished torebuild populations of depleted predatory fishstocks. Fauchald (2010) suggest that targeted har-vesting of herring in the North Sea could break thereinforcing feedback where large populations ofherring suppress cod recruitment through preda-tion on cod eggs and larvae. The Swedish Board ofFisheries has recently initiated a pilot project toinvestigate if targeted fishing of sprat (Sprattussprattus) can reverse the prey-to-predator loops thatlock Baltic cod (Gadus morhua) populations in a lowabundance state. However, targeted removals inpelagic systems could be confounded by highlydynamic population (stock) behavior, such as adultmobility and reproductive migration patterns, andcomplex food-web dynamics that can lead tounexpected outcomes. In the Northern Benguelacurrent, for example, anchovies (Engraulis capensis)were deliberately overfished in an attempt to bringback the economically more attractive, but collapsedsardine (Sardinops sagax) stock. This strategy failed,however, and resulted in an unexpected shift tobenthic anoxia (due to loss of suspension-feeding

Figure 4. A map showing examples of the global distri-bution of regime shifts in coastal pelagic food webs (A). Atable summarizes the location, identified driver(s) for theobserved shifts, and the feedbacks operating in thedegraded state (B). A graphic illustration of interactingfeedbacks (C): Eutrophication-related syndromes may bestabilized by increased phytoplankton, leading toincreased oxygen consumption, anoxia, and release ofphosphorus from anoxic sediments, further stimulatingphytoplankton production (A); anoxic conditions canreduce reproductive success of top predators, andreduced top predator abundances can lead to a cascadingincrease in phytoplankton (AP); top predator growth andrecruitment can be negatively affected by predation oneggs and larvae of predators, competition for zooplanktonprey, and size dependent growth (PP); jellyfish invasionsare facilitated by reduction of mesopredators, predationon (and competition with) mesopredators once estab-lished, and increased sexual success with increasingdensities (J).

b

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fish resulting in increased pelagic–benthic organicsincreasing the biological oxygen demand), demersallow-oxygen tolerant gobies (Utne-Palm and others2010), and a pelagic state dominated by ‘‘jellypredators’’ (Bakun and Weeks 2006).

WINDOWS OF OPPORTUNITY FOR BREAKING

FEEDBACKS

From the described cases, finding potential actionsto confront unwanted feedbacks is a challengingbut not insurmountable task, although breakingfeedbacks that are strong and operate at very largescales may be particularly difficult, regardless ofbiome. However, breaking feedbacks in degradedecosystems could benefit from naturally occurringpulse events that temporarily facilitate a redirectionof ecosystem processes. Such ideas have been pro-posed for arid ecosystems where exceptionally wetEl Nino (or La Nina)-years could assist in breakingfeedbacks that lock arid systems in a degraded state(that is, depleted vegetation biomass and soil ero-sion) (Holmgren and others 2001). Althoughreducing human activities initially causing theshift, such as overgrazing and wood harvesting, orextensive rain can lead to recovery, degraded aridstates are often very difficult to reverse due toreinforcing biotic–abiotic feedbacks associated withvegetation depletion, such as loss of protectiveshade and moisture for seedlings. Holmgren andothers (2001) suggest that if degraded areas are pre-conditioned by removing grazers and dispersingseeds before a predicted wet El Nino (or La Nina)-event arrives it increases the likelihood that seed-lings will grow sufficiently to become resistant todrought and grazing. As new canopy is formed,increasing moisture and shade will reinforce avegetated (desirable) state.Large-scale periodic environmental change could

potentially also help break strong feedbacks inmarine ecosystems. In the Baltic Sea, for example,recovery of collapsed cod stocks is partly hamperedby recruitment failure due to the widespread anoxicconditions caused by limited water exchange andeutrophication (Figure 4C). Special atmosphericconditions over the western Baltic Sea and north-east Atlantic (Lehmann and others 2004) can causehighly saline and extremely oxygen rich water toflow from the North Sea and effectively re-oxy-genate the deeper basins of the Baltic Sea. Suchexceptional inflows (the last event occurred in2003) could provide temporal windows of oppor-tunities for cod stock recovery by improving repro-duction conditions (Koster and others 2005). Taking

advantage of this natural opportunity requires aninstitutional framework that is able to mobilizequickly before the window closes (for example,putting a temporary ban on cod fishery).

CONCLUSIONS AND DIRECTIONS AHEAD

Many marine ecosystems have shifted intodegraded states and we have focused on a fewselected biomes. Although many of these shifts seempersistent, recent signs of recovery in, for example,over-exploited coastal pelagic marine systems indi-cate that such profound ecological changes are notirreversible (Frank and others 2011; Eero and others2012). Although science has mainly been concernedwith the causes of shifts into degraded states, andhow to avoid them, more focus needs to be chan-neled toward understanding what mechanisms (thatis, feedback dynamics) that prevent/delay therecovery from these states and finding ways to breakthem (Hughes and others 2010). To facilitate futurework to improve our understanding of these issues,we formulate our main conclusions into four broadresearch challenges.

(1) Identifying and understanding the feedbacks thatmay cause ‘‘lock in’’-effects of degraded marine ecosystemstates

We show how some degraded marine states arereinforced by multiple feedbacks that can interactand form complex synergies. Degraded states ofcoral reefs and kelp are primarily maintained bybiotic feedbacks whereas degraded states in seagrassbeds, and coastal pelagic food webs are character-ized by strong biotic–abiotic feedbacks. In othercases, there is a mixed situation, such as in oysterreefs, where feedbacks involve both biotic andabiotic processes. To better understand lock in-ef-fects, future research needs to more exhaustivelyidentify feedbacks in a broader range of degradedmarine states, and learn how these feedbacksinteract in space and time. Qualitative descriptionsneed to be complemented by quantitative assess-ments of feedbacks (that is, well-designed experi-ments) and long-term monitoring of variables thatinfluence feedbacks (for example, Carpenter andothers 2011). Together this could help developand parameterize models (for example, Mumbyand others 2007) to better quantify and test therelative importance of different feedbacks, andidentify leverage points for breaking them. There isalso an urgent need to better understand how slowdrivers of change, such as elevated seawater tem-perature and ocean acidification, may influencemarine threshold dynamics and increase the risk of

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triggering reinforcing feedbacks (Bertness andLeonard 1997).(2) Develop management actions geared at breaking

feedbacksContemporary management approaches may,

deliberately or unintentionally, manipulate feed-backs. In most cases, however, single feedbacks aretargeted/influenced. We suggest that there is nosingle-feedback management solution for breakingout of degraded marine states. Multiple feedbackswill have to be addressed in tandem and may needto be unlocked in specific sequences. Because of thecomplex dynamics of ecosystems, interventionsgeared at breaking feedbacks may generate unex-pected outcomes (Bakun and Weeks 2006).Manipulating feedbacks to reverse degraded mar-ine states will require an experimental approachcoupled with regular monitoring, that is, to enable‘‘learning through doing’’ within an adaptivemanagement framework.(3) Understand how feedbacks in natural systems

interact with socioeconomic processesThe changes in ecosystem feedbacks described

here are essentially inflicted by human drivers (forexample, overfishing, eutrophication, and climatechange), and the social dynamics surrounding them,including markets, poverty, and governance struc-tures (Cinner and others 2009a). At the same time,the social dynamics are shaped by the ecologicalchanges they produce (for example, manifestedthrough changes in ecosystem services). Although adeeper treatment of this issue is beyond the scope ofthis mini-review, understanding how feedbacks innatural systems interact with socioeconomic factorsis crucial for steering degraded marine ecosystemstoward improved conditions. For example, syner-gistic effects between degraded ecosystem states andsocial processes have been described in small-scaleartisanal coral reef fisheries in Kenya (Cinner andothers 2009b). In a response to diminished fishyields, fishing effort among the poorest increasedtogether with a switch toward more effective anddestructive fishing gears, such as beach seine netsand dynamite. These gears have significant impactson the ecosystem by catching fish indiscriminately(with regards to size, species, and ecological func-tion) and severely damaging the coral reef frame-work (that is, fish habitat). This reinforces ecologicalfeedbacks that maintain an undesirable coral reefstate, reduces future fish catches and increasespoverty in the long-term. Escaping this ‘‘social–ecological trap’’ (Steneck 2009), has proven verydifficult (Cinner and others 2009a). Similar syner-gies between social and ecological process occur alsoin rich industrialized countries (although the drivers

may be different) but are often effectively camou-flaged by technological advancements, exploitationof species at lower trophic levels, serial exploitationof fishing grounds, subsidies, and trade (Berkes andothers 2006; Frank and others 2005; Steneck andothers 2011).

Because most current approaches to governanceand management of marine ecosystems havefailed to adequately link social and ecologicalprocesses (Hughes and others 2005) transforma-tions of existing management regimes are required(Gelcich and others 2010). Although transforma-tions may be necessary to escape undesirablesocial–ecological pathways (for example, social–ecological traps) they need to be carefully navi-gated because the outcomes are uncertain.Consequently, successfully breaking out ofdegraded marine states requires a better under-standing of the socioeconomic drivers causingchanges in ecological feedbacks, but also of howecosystem changes lead to correspondent altera-tions in human behavior, institutional frame-works, and policy. To capture and quantify thesecross-systemic interactions, novel transdisciplin-ary research frameworks (Folke 2006) and ana-lytic tools that integrate qualitative andquantitative ecological and social science data arerequired (for example, Cinner and others 2009a).

(4) Utilizing windows of opportunity to escape unde-sirable ecological and social–ecological states

Breaking strong ecological feedbacks and escapingsocial–ecological traps will require complex actionplans, which may be very costly and time consum-ing. This process could be aided by certain events,windows of opportunity, which act as a catalyst fordirected change. Such events could be fairly pre-dictable, such as annual storms, El Nino-years, andcycles of political terms and could be embedded inmanagement strategies aimed at reversing degradedmarine ecosystem states. In other cases, opportuni-ties are unpredictable, such as exceptionally good/bad years of reproduction, unforeseen storms, sud-den die-off events, political and economic turmoil.Harnessing the benefits of these events requiresflexible institutional and management frameworksthat allow for a rapid response when an opportunityarrives.

The idea of windows of opportunity as facilitatorsof desirable change is novel but we are still far froma comprehensive understanding. Future work needsto identify what constitutes windows of opportu-nity, how far we can go in anticipating them, andhow social–ecological systems can be prepared so asto channel their effect with directed actions aimed atforcing unwanted feedbacks.

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ACKNOWLEDGMENTS

T.B. and H.O. are supported by an EC FP7 project(Grant No. 226675), the strategic FORMAS projects(grant no 2009-252) and ‘‘Baltic EcosystemApproach to Management.’’ J.S.E. was funded byFORMAS (Grant Nos. 2008-839 and 2009-1086).M. de la T.C. is funded by the Swedish Interna-tional Development Cooperation Agency (Sida).R.S.S. was funded from the National Fish andWildlife Service, Smithsonian Institution andU. Maine Sea Grant program. We are very gratefulfor constructive comments provided by threereviewers. Mistra supported this research through acore grant to the Stockholm Resilience Centre.

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