Paradigms in the Recovery of Estuarine and CoastalEcosystems

Carlos M. Duarte & Angel Borja & Jacob Carstensen &

Michael Elliott & Dorte Krause-Jensen & Núria Marbà

Received: 4 July 2013 /Revised: 30 November 2013 /Accepted: 2 December 2013# Coastal and Estuarine Research Federation 2013

Abstract Following widespread deterioration of coastal eco-systems since the 1960s, current environmental policies de-mand ecosystem recovery and restoration. However, vaguedefinitions of recovery and untested recovery paradigms com-plicate efficient stewardship of coastal ecosystems. We criti-cally examine definitions of recovery and identify and test theimplicit paradigms against well-documented cases studiesbased on a literature review. The study highlights a need formore careful specification of recovery targets and metrics forassessing recovery in individual ecosystems. Six recovery

paradigms were identified and examination of themestablished that partial (as opposed to full) recovery prevails,that degradation and recovery typically follow different path-ways as buffers act to maintain the degraded state, and thatrecovery trajectories depend on the nature of the pressure aswell as the connectivity of ecosystems and can differ betweenecosystem components and among ecosystems. A conceptualmodel illustrates the findings and also indicates how restora-tion efforts may accelerate the recovery process.

Keywords Estuarine . Recovery . Paradigms

Introduction

Growing evidence of the widespread deterioration of coastalecosystems due to increased inputs of materials, such asnutrients, organic matter, sediments, and pollutants; physicaldisturbance through shoreline and offshore constructions; andtrawling fisheries among others, has led to policy decisionaiming, directly or indirectly, to improve the status of ourcoastal ecosystems. Examples of these policies include theEuropean Water Framework Directive (WFD, 2000/60/EC)and the Marine Strategy Framework Directive (MSFD,2008/56/EC), the Clean Water Act (CWA) and the NationalEstuary Program (www.epa.gov/nep) in the USA, and therecently announced UN Oceans Compact (www.un.org/Depts/los/ocean_compact/oceans_compact.htm).

Many of these statutory instruments work on the simplepremise of assessing whether the status of a system is asexpected and if not then requiring management measures torestore the system (Mee et al. 2008). Regulatory measures settargets for the recovery process (Borja et al. 2012), which inturn demand an understanding of the trajectories of recovery,and the traits that allow determining when coastal ecosystemscan be declared recovered (Elliott et al. 2007). However, the

Communicated by Wayne S. Gardner

C. M. Duarte (*) :N. MarbàDepartment of Global Change Research, IMEDEA (CSIC-UIB),Institut Mediterrani d’Estudis Avançats, Miquel Marquès 21,07190 Esporles, Illes Balears, Spaine-mail: carlosduarte@imedea.uib-csic.es

C. M. DuarteFaculty of Marine Sciences, King Abdulaziz University, P. O. Box80207, Jeddah 21589, Saudi Arabia

C. M. DuarteThe UWA Oceans Institute, University of Western Australia, 35Stirling Highway, 6009 Crawley, WA, Australia

A. BorjaMarine Research Division, AZTI-Tecnalia, Herrera Kaia, Portualdeas/b, 20110 Pasaia, Spain

J. CarstensenDepartment of Bioscience, Aarhus University, Frederiksborgvej 399,4000 Roskilde, Denmark

D. Krause-JensenDepartment of Bioscience, Aarhus University, Vejlsøvej 25,8600 Silkeborg, Denmark

M. ElliottInstitute of Estuarine & Coastal Studies, University of Hull,Hull HU6 7RX, UK

Estuaries and CoastsDOI 10.1007/s12237-013-9750-9

scientific input demanded by regulators in applying theseinstruments for the efficient stewardship of coastal ecosystemsappears not to be as simple and straightforward as expected,providing an impetus for research on the recovery of coastalecosystems.

Stress ecology, aimed at understanding the responses ofecosystems to stressors, developed as a research programduring the 1970s and 1980s as pressures on the environmentincreased (Odum 1985). Subsequent efforts to alter and re-verse deterioration of coastal and estuarine ecosystems led tothe development of recovery ecology (Lotze et al. 2011).However, few examples of successful ecosystem recoveryare available to date (e.g., Jones and Schmitz 2009; Borjaet al. 2010; Greening et al. 2011; Lotze et al. 2011; Orth andMcGlathery 2012), with most examples focused on recoveryof populations (Lotze et al. 2011) and, at most, habitats (Elliottet al. 2007), but not ecosystems (Duarte et al. 2009;Steckbauer et al. 2011).

Ecosystem restoration is more challenging than biologicalconservation, where the target is to recover a species or habitatof interest rather than an ecosystem, as the targets for ecosys-tem restoration involve both structural and functional attri-butes. However, both are often confounded (Lotze et al.2011). Available examples of coastal ecosystem recoveryshow, for instance, that recovery is rarely complete and is aslow process involving several decades (Borja et al. 2010;Duarte et al. 2009; Lotze et al. 2011; Steckbauer et al. 2011;Verdonschot et al. 2013). The conceptual model proposed byElliott et al. (2007) indicates that in many cases other habitatsare created which may approximate but not replicate thatwhich was originally lost. This is particularly the case wherestatutory instruments require compensatory habitat to be cre-ated to accommodate habitat loss due to human activities suchas the building of a new port.

The paucity of observations on the recovery of estuarineand coastal ecosystems has led to recovery ecology beingguided by theory (Lotze et al. 2011). However, theory needsbe confirmed by observations, and thus, the theoretical under-pinnings of marine recovery ecology remain primitive, andoften draw from assumed axioms and circular reasoning. Forinstance, the recovery of coastal and estuarine ecosystems hasbeen suggested to depend on the removal of the pressure(Jones and Schmitz 2009; Lotze et al. 2011), and evolve froma rudimentary structure first to a more optimal state later(Thom et al. 2012). It has been assumed that if the suitablephysicochemical environment, i.e., the boundary conditions,is created then the natural ecology will develop (Elliott et al.2007; Simenstad et al. 2006). Ecosystem recovery has beenclassified into complete recovery, partial recovery, and norecovery (Lotze et al. 2011) and has been argued to be depen-dent on ecosystem recoverability defined as the ability of ahabitat, community or individual (or individual colony) ofspecies to redress damage sustained as a result of an external

factor (Elliott et al. 2007). Despite this, no guidance has beenprovided as to what determines ecosystem recoverability orhow to assess whether recovery has been achieved.

Assessing when the recovery process has reached an endpoint is nontrivial, as baselines are dynamic and changethrough time (Jackson et al. 2001; Mee et al. 2008; Duarteet al. 2009; Carstensen et al. 2011) and may not be reachedsimultaneously for different indicators of ecosystem status(Borja et al. 2010). Similarly, there is the need to be especiallyclear what characteristics are required to indicate that ahealthy, fully-functioning ecosystem has been achieved (Tettet al. 2013). The expectation that recovery is simply theinverse process of deterioration through reversible trajectoriesproved too naïve, since there is now ample evidence thateutrophication (Duarte et al. 2009), hypoxia (Steckbaueret al. 2011), and overfishing (Jackson et al. 2001) are not fullyreversible processes. Indeed, coastal ecosystems follow com-plex trajectories and exhibit hysteresis during recovery (Elliottet al. 2007; Duarte et al. 2009). In addition, coastal andestuarine systems are inherently variable, which make thedetection of both degradation and recovery more difficult(Elliott and Whitfield 2011). Growing frustration with failureof recovery efforts to meet targets may act as a deterrent toengage society in further efforts to restore coastal ecosystems.

Failure to acknowledge and anticipate the trajectories ofrecovering ecosystems or even diagnose whether an ecosys-tem has recovered generate considerable unrest to environ-mental managers and society. Diagnosing whether an ecosys-tem has recovered may require a defined state, often summa-rized as “good” (Mee et al. 2008), but this is of little use if thestatus is poorly defined or has a large subjective element (Tettet al. 2013). Developing objective and precise definitions ofrecovery is not only a matter of academic interest, given thatthe restoration of estuarine and coastal ecosystems now carryconsiderable financial and legal repercussions. For example,developers may be required to invest considerable funds torestore habitats or at least to produce compensatory areas fordamaged habitats; similarly, states and developers may be inbreach of statutory instruments if they cannot demonstraterecovered ecosystems. Hence, the scientific underpinning ofefforts to restore estuarine and coastal ecosystems must berapidly improved and a new framework guiding these effortsthat acknowledges and faces the complexities involved needbe established.

Here, we offer a “conceptual model” of the recovery ofestuarine and coastal ecosystems. We do so by first criticallyexamining current definitions of recovery, and identifying andtesting the implicit paradigms and beliefs against well-documented cases of responses of coastal and estuarine eco-systems to restoration efforts. This is based on a review of theliterature on recovery of estuarine and coastal ecosystems,which is dominated by studies focused on benthic systemsand fish. The term paradigm is used here sensu lato , as a

Estuaries and Coasts

Table 1 Examples of definitions of recovery (in some cases referred to asrestoration), the type of metric use to assess recovery (ecosystem struc-ture, ecosystem function, ecosystem services, and undefined standards),the recovery target used in the definition (baseline referring to

predisturbance levels, baseline adjusted for human activities, baselinereferring to resilience/resistance/sustainability/integrity, baseline unde-fined) and the reference citing the definition

Definition Metric Target Reference

The return of key variables to the preperturbation state Undefined standards Baseline at/nearpredisturbance level

Jones and Schmitz (2009)

A return to predisturbance conditions Undefined standards Baseline at/nearpredisturbance level

Kraufvelin et al. (2001);Lardicci et al. (2001);Kaiser et al. (1988)

Realistic baselines (for estuarine restoration) must beestablished at a post-industrial starting point

Baseline adjusted forhuman activities

Weinstein (2007)

The desired outcome of any ecosystem approach isnot only to restore and rehabilitate the health,productivity and biodiversityof ecosystems but also the overall quality of humanlife through a resource management approach thatis fully integrated with social and economic goals

Ecosystem structureEcosystem functionEcosystem services

Baseline adjusted forhuman activities

Weinstein (2007)

An obvious improvement as shown by communityand environment variables

Undefined standards Increase/improvement Moore and Rodger (1991)

Restoration was assessed relative to targets for seagrassextent based on predisturbance levels

Ecosystem structure Baseline at/nearpredisturbance level

Orth et al. (2010)

Recovered seagrass meadows were persistent and ableto adjust to changing conditions; they were healthy[as shown by shoot characteristics and growth parameters]

Ecosystem structureEcosystem function

ResistanceResilience

Park et al. (2009)

Recovery was related to a significant increase in speciesrichness and cover of macroalgae

Ecosystem structure Increase/improvement Piazzi and Ceccherelli (2006)

Recovery was defined as benthos attaining a climax community Undefined standards Increase/improvement Rosenberg et al. (2002)

Ecological restoration is the process of assisting the recoveryof an ecosystem that has been degraded, damaged,or destroyed

Temperaton et al. (2004)

These attributes [showing recovery] include the capacity ofthe physical environment to sustain reproducing populations,the integration with the landscape, and self sustainability

Ecosystem function Resilience Ruíz-Jaén and Aide 2005

A close approximation of its condition prior to “disturbance”which requires “reestablishment” of predisturbance aquaticfunctions and related physical, chemical, and biologicalcharacteristics

Ecosystem structureEcosystem function

Baseline at/nearpredisturbance level

NRC (1992) (see alsoSimenstad et al. 2006)

Restoration as seeking to establish “a site that is self-regulatingand integrated within its landscape, rather than to reestablishan aboriginal condition that can be impossible to define and/or restore within the context of current land use or global change”

Resilience Middleton 1999 (see alsoSimenstad et al. 2006)

The benthic community in an area was assumed to be in a stateof near recovery from trawling when the biomass (B)or production (P) reached 90 % of predicted biomass thatwould occur in the absence of trawling (B0.9 or P0.9). This 90 %value was chosen arbitrarily as a value that was close to thepristine state

Ecosystem structureEcosystem function

Baseline at/nearpredisturbance level

Hiddink et al. (2006)

Restoration targets must be defined based on ecological and culturalknowledge=ecocultural restoration. (“..ourvalues toward those ecosystems will shift over time asthey have been doing throughout history”)

Baseline adjusted forhuman activities

Higgs (2005)

Recovery (of fish populations) implies reaching a targetlevel of abundance

Ecosystem structure Baseline unspecified Hutchings and Rangeley(2011)

Recovery of an ecosystem is characterized by the re-establishment of a biological community in which theplants and animals characteristic of that communityare present and functioning normally

Ecosystem structureEcosystem function

Kingston (2002)

The restoration process or trajectory reestablishes adynamically stable ecosystem that is fully developedstructurally and functionally and is resistant and resilientto disturbances

Ecosystem structureEcosystem function

ResistanceResilience

Thom et al. (2012)

Undefined standards Lotze et al. (2011)

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pattern or model (Oxford Dictionary), and not in the morerestricted form of a Khunian paradigm (1962).

Definitions of Coastal Ecosystem Recovery

The concept of ecosystem recovery draws from health sci-ences to embed a concept of damage to the health or integrityof an ecosystem (Tett et al. 2013). For instance, the journalAquatic Ecosystem Health and Management focuses on thehealth of freshwater, marine, and estuarine ecosystems withthe objective to promote an understanding of the functioningof ecosystems, the remediation, healing, recovery, and resto-ration of stressed environments from the impact of anthropo-genic stresses (www.aehms.org/journal.html#objectives).Unfortunately, both the concept of ecosystem recovery andhealth involve much vagueness and circular reasoning, such asecosystem health defined as the absence of signs of ecosystemdistress (Costanza 1992). In turn, healthy ecosystems have beendescribed as those being “stable and sustainable, maintaining itsorganization and autonomy over time and its resilience to stress”(Rapport et al. 1998; Tett et al. 2013). Implicitly, ecosystemrecovery implies returning a distressed ecosystem to a healthycondition. Unfortunately, these definitions are not easy tooperationalize, which underlines difficulties to ascertain whetheran ecosystem has recovered from stress.

A recent review (Lotze et al. 2011) acknowledged thediversity of definitions of coastal ecosystems and suggestedthat the definition is better described by the different metricsused to assess recovery. Indeed, many explicit or implicitdefinitions for the recovery of coastal ecosystems have beenproposed (Table 1). Examination of these definitions showsthat they focus on various combinations of a restricted set ofmetrics and targets. Metrics used to define recovery focus onmarine ecosystem structure (e.g., species abundance, 36 %),function (e.g., growth, 28 %), or services (e.g., nutrient cy-cling, 8 %), while a significant number of definitions are notprescriptive as to the metric to be used to diagnose recovery(28 %). Recovery is defined as the achievement of a particular

target in those metrics. These targets can involve a baseline,which can refer to predisturbance levels or include an allow-ance for tolerable deviations due to human activities; a trend,such as an increase or improvement in the metric; or a partic-ular response to disturbance, such as resistance (the ability towithstand stressors) or resilience (the ability to return to theprevious stable state following disturbance). Most definitionsfocus on targets based on baselines (54 %), whetherpredisturbance or allowing for some human interference, andmany also focus on resilience (25 %). The emphasis onresilience rests on the belief that this property, regarded asthe ability to absorb stress perturbations, is a trait characteristicof healthy ecosystems (Elliott et al. 2007). However, somedefinitions remain vague as to the target of restoration efforts(e.g., Kingston 2002).

Legislative frameworks, such as the WFD or CWA usemetrics and targets of environmental/ecological status to man-age pressures on aquatic ecosystems—indeed, it is axiomaticthat “if you cannot measure it then you cannot manage it”. TheWFD equates healthy ecosystems with those showing “goodecological status”, and have formulated a number of metricsfor “good ecological status” around Europe, most of thembased on ecosystem structure (Hering et al. 2010), togetherwith some tolerable deviations. Whenever coastal ecosystemsfall below good status (i.e., is assessed as having moderate,poor, or bad status), managers are obliged to take action to re-establish a “good status” of the ecosystem.

Large, multibillion dollar coastal restoration programs areongoing in the Gulf of Mexico to restore ecosystems impactedby the oil spill associated with the Macondo well blow out.These efforts follow the Natural Resources DamageAssessment (NRDA) process under two laws in the USA,the Comprehensive Environmental Response, Compensationand Liability Act (CERCLA) and the Oil Pollution Act. TheNRDA process involves a primary restoration action to returninjured resources to baseline conditions and a compensatoryrestoration action to compensate for the interim loss of ser-vices pending return to baseline conditions (cf. http://www.epa.gov/superfund/programs/nrd/nrda2.htm).

Table 1 (continued)

Definition Metric Target Reference

In practice, recovery is often measured as some form ofincrease, improvement or shift in certain response variables,ideally reversing to predisturbance conditions

Baseline at/nearpredisturbance level

The process of re-establishing, following degradation byhuman activities, a sustainable habitat or ecosystem witha natural (healthy) structure and functioning

Ecosystem structureEcosystem function

Sustainability Elliott et al. (2007)

The process of assisting the recovery and management ofecological integrity. Ecological integrity includes a criticalrange of variability in biodiversity, ecological processes andstructures, regional and historical context, and sustainablecultural practices

Ecosystem structureEcosystem function

Integrity Bradshaw (2002)

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Paradigms of Coastal and Estuarine Ecosystem Recovery

Most importantly, the literature on the recovery of coastal andestuarine ecosystems has expanded rapidly, at 15.4 % year−1,since 1980 (Fig. 1), accumulating evidence of a number ofparadigms that represent constructs as to the trajectories ordrivers of ecosystem recovery (Table 2; see also Elliott andWhitfield 2011). These paradigms refer to the magnitude,type, and frequency/timing of the pressures supported, therole of ecosystem structure and connectivity in affecting theoutcome of recovery efforts, and the trajectories of recoverytowards baselines.

Paradigm 1. Recovery of Marine Ecosystems is Idiosyncratic

Ecosystem structure is believed to affect the recovery ofmarine ecosystems. For instance, biotic factors and interac-tions are believed to affect recovery trajectories, positively ornegatively, rendering these highly idiosyncratic (Table 2;Perkol-Finkel and Airoldi 2010; Rosenberg et al. 2002).Moreover, biotic interactions are dependent orsuperimposed on and ultimately influence physicochem-ical factors and interactions, thereby further enhancingidiosyncrasy (Gray and Elliott 2009). Recovery timescales are expected to be dependent on the specificcommunity affected and the magnitude of the impacts,such that changes in habitats, for instance, are expectedto delay recovery (Table 2). Evidence of idiosyncraticrecovery has been derived, for instance, from observa-tions of divergent trajectories and outcomes of recover-ing macrophyte beds within different areas of an estuaryfollowing nutrient reduction plans (Orth et al. 2006).This paradigm implies that recovery is highly variableand essentially unpredictable.

Species traits may be able to provide clues to recov-ery processes. For instance, a long-held tenet is thatrecovery involves a succession from r-strategist to k-strategist species (e.g., Dolbeth et al. 2007). This obser-vation compares to arguments that ecosystems dominat-ed by long-lived, large, k-strategists species often re-quire longer time scales to recover than those dominatedby short-lived, small, r-strategist species (e.g., Kingston2002; Jones and Schmitz 2009; Lotze et al. 2011).Hence, ecosystems, such as estuaries, which have natu-rally large populations of stress-tolerant strategists, mayrecover relatively fast (Elliott and Whitfield 2011).Recovery also often follows a pathway by which envi-ronmental conditions recover first, followed by primaryproducers and lastly consumers (Borja et al. 2010).However, this pattern is not always observed, and envi-ronmental variables can recover in parallel to communi-ties (Jones and Schmitz 2009).

Paradigm 2. Ecosystem Function is Easier to Recoverthan Ecosystem Structure

Whereas indeed recovery of marine ecosystems can be oftenidiosyncratic when focusing on ecosystem structure, there isevidence that ecosystem function recovers relatively rapidly,with the consequences that recovery efforts sometimes lead todifferent species composition in the communities, but withsimilar functional traits to those existing prior to disturbance(Norkko and Bonsdorff 1996). Indeed, that ecosystem func-tion seems to be more stable and robust, i.e., shows morehomeostasis (Odum 1985), than ecosystem structure has longbeen argued to characterize the response of ecosystems tostress (Odum 1985). However, there are dissenting views inthat ecosystem function is sometimes slower to recover thanstructure (Ruíz-Jaén and Aide 2005).

Paradigm 3. Degradation is Fully Reversible

Some authors, as well as many management and legislativeframeworks, such as the WFD and the NRDA process, im-plicitly or explicitly assume degradation to be a fully revers-ible process, with recovery reaching predisturbance or base-line status (e.g., Dolbeth et al. 2007; Jones and Schmitz 2009).There is, however, considerable debate and disagreement onthis paradigm as degradation can be, in some cases, irrevers-ible (Lotze et al. 2011). The reversibility of degradation pro-cesses may involve an element of time scales, for it can beargued that some ecosystems will eventually return to theoriginal status, but so slowly that degradation is consideredirreversible in management time scales. For instance, slow-growing seagrass, Posidonia oceanica meadows have beenshown to display little recovery from trawling after 100 years(González-Correa et al. 2005), and models indicate that re-covery of these meadows require many centuries (Duarte1995). Possibly the only truly irreversible degradations arethose involving species extinction, such as the extinction ofthe Steller’s sea cow following intense hunting in the 1800s(Turvey and Risley 2006). Moreover, shifting baselines due tolarge-scale environmental changes, such as climate change orincreased UVB radiation, during the degradation and recoveryprocess has been argued to lead to deviations from thepredisturbance ecosystem status following recovery ofeutrophied coastal ecosystems (Duarte et al. 2009;Carstensen et al. 2011). Villnäs et al. (2011) reported thatshifting baselines in community structure affected the defini-tion of reference conditions in the recovery of benthic systemsimpacted by aquaculture.

Recovery often involves the transition of coastal ecosys-tems across alternative stable states. However, the number ofalternative stable states is not necessarily just two, a degradedand a healthy state, and recovery efforts have sometimesfound that the ecosystems recover to a different alternative

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stable state than that present prior to disturbance (Munkes2005). This is compounded further as coastal and estuarineecosystems are arguably more dominated by gradients, bothof biological and physicochemical elements, and multipleecotones, with each part of that continuum being stable underdiffering time scales.

Paradigm 4. Degradation and Recovery Follow Similar,but Opposite, Trajectories

Degradation and recovery trajectories are similar, but oppo-site. This is often assumed in regulatory frameworks, such asthe WFD (Hering et al. 2010). However, most evidence avail-able contradicts this paradigm. Degradation and recoverytrajectories generally differ from degradation ones due toshifting baselines and hysteresis (Duarte et al. 2009), and thereconfiguration of ecosystem buffers (Lardicci et al. 2001;Elliott et al. 2007; Taylor et al. 2011; Villnäs et al. 2011;Krause-Jensen et al. 2012). The consequence is that thresholdsseparating alternative states often differ between ecosystemdegradation and recovery, with the consequence that degrada-tion and recovery trajectories follow different paths resultingin nonlinear relations between ecosystems status and pressure(Elliott et al. 2007; Duarte et al. 2009; Borja et al. 2010;Fig. 2). Time lags in ecosystem responses to the removal ofpressures responsible for degradation are often reported,resulting in hysteresis (Perkol-Finkel and Airoldi 2010). Forinstance, nutrient reduction plans often fail to return coastalecosystems to the predisturbance state due to hysteresis andshifting baselines (Duarte et al. 2009), and recovery fromhypoxia often shows hysteresis and long-time lags(Steckbauer et al. 2011), which render the assessment ofrecovery difficult (Duarte et al. 2009).

Fig. 1 Number of papers on estuarine and coastal recovery publishedannually. Data obtained from the Web of Science (accessed June 3, 2013)using the search string (Estuar* OR Coast*) AND (recovery OR restoration)

Table 2 Overview of paradigms on the trajectories or drivers of ecosystem recovery expressed explicitly or implicitly in the literature

Paradigms Evidence in support/opposition to paradigm

1. Recovery of marine ecosystems isidiosyncratic

Supporting Species traits and interactions render recovery trajectories and outcomes unpredictable

Opposing Predictable patterns have been reported with small, fast-growing r-strategists speciesrecovering fast and large, slow-growing k-strategists being slow to recover

2. Ecosystem function is easier to recoverthan ecosystem structure

Supporting Although ecosystem structure may differ from the baseline after recovery, functions are oftensimilar

Opposing Ecosystem function has been observed to recover more slowly than ecosystem structure insome cases

3. Degradation is fully reversible Supporting Recovered ecosystems have been shown to reach pre-disturbance status in some cases

Opposing A review of the extent of recovery of estuarine and coastal ecosystems showed that partialrecovery prevails

4. Degradation and recovery followsimilar but opposite trajectories

Supporting Parallel degradation and recovery trajectories have not yet been observed in coastal andestuarine ecosystems

Opposing Recovery trajectories always show hysteresis due to the presence of buffers that slow downrecovery and differential thresholds between the degradation and recovery phases

5. Recovery depends on the characteristicsof the pressure

Supporting Overwhelming evidence shows that recovery depends on the type, magnitude, frequency andtiming of the pressures

Opposing No studies provide evidence of independence of recovery of the characteristics of the pressure

6. Connectivity accelerates recovery Supporting All available evidence along with theory point at connectivity being essential for the recoverythrough the supply of propagules and colonizers.

Opposing No evidence suggests that connectivity does not play a role in recovery.

The paradigms refer to the magnitude, type and frequency/ timing of the pressures supported, the role of ecosystem structure and connectivity in affectingthe outcome of recovery efforts, and the trajectories of recovery towards baselines. For each paradigm, supporting and opposing evidence is summarizedand where there is a clear overweight of supporting or opposing evidence, this is indicated in bold

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Paradigm 5. Recovery Depends on the Characteristicof the Pressures

Recovery is believed to be dependent on the characteristics ofthe pressures conducive to degradation, particularly their type,magnitude, frequency, and timing relative to key ecosystemevents and stages (Jones and Schmitz 2009; Taylor et al. 2011;Villnäs et al. 2011; Lotze et al. 2011). Recovery times havebeen argued to be directly related, for any one ecosystem type,to the severity of the disturbance (Schaffner 2010), and to beslower when the disturbance is anthropogenic than for naturaldisturbance (Jones and Schmitz 2009). Recovery then de-pends on the ability of the stressor-receiving environment toabsorb and assimilate the stressor, for example recovery froma degrading waste (e.g., sewage and oil) is likely to be fasterthan from a nondegrading one such as metal pollution; thelatter requires sequestration/burial to remove the stressor.Recovery will also proceed faster if the pressure is reducedbefore the main annual recruitment period than after this event(Borja et al. 2010).

Paradigm 6. Connectivity Accelerates Recovery

Recovery is believed to be dependent on connectivity betweenthe degraded ecosystem and healthy adjacent ecosystems. Forinstance, the availability and import of propagules affect therecovery ofmarine ecosystems (Pratt 1994). Connectivity thusaffects the structural trajectories of recovering ecosystems byinfluencing colonization patterns and pioneer assemblages(Norkko and Bonsdorff 1996). Connectivity also affects func-tional aspects of recovery through influence on the resistanceand resilience of ecosystems (Elliott et al. 2007; Gaines et al.2010), where resistance is defined as the ability to withstand astressor before adverse changes occur and resilience is definedas the ability to return to the previous stable state followingdisturbance. There is ample consensus on this paradigm,which is supported by solid evidence, as well as theory(Gaines et al. 2010; Elliott and Whitfield 2011).

In summary, paradigms 5 (the dependence of recovery onthe characteristics of the pressures) and 6 (the importance ofconnectivity for recovery) are strongly supported by observa-tions (Table 2). Two paradigms, paradigms 3 (recovery can bea full reversal of degradation) and 4 (degradation and recoveryfollow similar but opposite trajectories) should be rejected,with some evidence still supporting paradigm 3 though partialrecovery prevails, but no evidence supporting paradigm 4(Table 2). Paradigm 3 could thus be modified to indicate thatwhile some recovery of an ecosystem state is always likely, itshould not be assumed that the recovered state equals thepredisturbance situation. Lastly, paradigms 1 and 2 have bothsupporting and opposing evidence. Whereas indeed speciestraits and interactions render recovery rather idiosyncratic, aspostulated in paradigm 1, there are indeed patterns that can be

used to formulate useful predictions (Table 2). Paradigm 2,that ecosystems function recovers prior to structure, has bothcomparable supporting and opposing evidence (Table 2).

Recovery vs. Restoration of Coastal and EstuarineEcosystems

Ecosystem recovery involves the recovery of structure andfunction following the removal of the stress, whether naturalor anthropogenic. This may be a passive process (merely withthe stressor naturally removed such as self-cleaning after anoil spill) or an active removal of the stress. In contrast, resto-ration always involves the deliberate (active) attempt to cata-lyze recovery. Whereas the removal of the stress is a criticalrequisite for restoration, ecosystem restoration typically ex-tends beyond stress alleviation to include additional interven-tions conducive to accelerated recovery.

The ecosystem response to pressures often involves shiftsbetween alternative states when a threshold of pressure hasbeen exceeded (Fig. 2). Despite this, most marine ecosystemsreceive multiple pressures, which may act in a synergisticmanner to stress the ecosystem, such that action on one pressurealone (e.g., nutrient reduction) may not be conducive to recov-ery when other pressures (e.g., overfishing, dredging, climatechange, or pollution) have not been removed (Stelzenmülleret al. 2010). An adequate understanding of the role of multiplepressures on ecosystem degradation is, therefore, necessary toidentify the conditions conducive to recovery.

Eco

syst

em s

tate

Pressure

A

B

C

Degradationtrajectory

Recovery trajectories

Threshold for recoveryThreshold for degradation

+ Restoration

No restoration

Fig. 2 Left to right Schematized trajectories of ecosystem response toincreasing pressure (red) showing degradation from a predisturbance state(A) to a degraded state (B) upon exceeding a pressure threshold. Right toleft Trajectories of ecosystem response to decreasing pressure (green)operating through an initial “lag/hysteresis phase” where buffers maintainthe degraded state followed by a recovery phase which, over time, leads tothe recovered state (C) as pressures are further reduced. Gray lines therecovery phase for a situation where restoration efforts are applied tofacilitate recovery (+ Restoration) as opposed to a situation without suchinitiatives (No restoration). The identified paradigms (Table 2) refer to therecovery trajectories

Estuaries and Coasts

Restoration efforts involve supplementing the natural pro-cess for recovery to be accelerated and/or achieve a statuscloser to the baseline, for example the artificial re-aeration ofthe Thames Estuary, London, accelerated the recovery of theestuarine fish community towards the historical baseline(McLusky and Elliott 2004), and the regulation of freshwaterinflow to the San Francisco Delta catalyzed the recovery ofvulnerable fish species of concern (Kimmerer 2002).Extended experience at ecosystem restoration has also providedsome clues to successful approaches, which represent the foun-dations of a new discipline, coastal eco-engineering, focused onsolutions to achieve recovery (Mitsch 2012; Simenstad et al.2006). In many examples of estuarine and coastal degradation,restoration has not been exerted/enforced. For instance, eutro-phication or hypoxia are often managed through the simpleremoval of the stress (nutrient and organic inputs), without anyfurther actions to catalyze recovery. However, some actions arepossible, such as manipulations of the biotic structure or thephysical or chemical conditions.

Biotic manipulations involve the recovery of target popu-lations, through the transplant or reintroduction of seagrasses(e.g., van Katwijk et al. 2009; Orth and McGlathery 2012),salt marsh plants (Mazik et al. 2010), mangroves (Greeninget al. 2011), or algae (Perkol-Finkel and Airoldi 2010). Theintroduction of target populations should consider the geneticstructure of the donor populations, as the success of theseintroductions may depend on the vigor and genetic diversityof the introduced specimens (van Katwijk et al. 2009;Frankham 2010). Successful biotic manipulations may alsoinvolve the introduction of additional engineer species able toimprove environmental conditions, such as the establishmentof oyster reefs or mussel populations to filter out particles andincrease water transparency, and the use of wetlands andmacroalgal cultures as biofilters of nutrients (Greening et al.2011). However, the success of manipulations involving trans-plants or introductions is critically dependent on the selection ofsuitable habitats (van Katwijk et al. 2009). Removal of invasivespecies, such as Caulerpa species in the Mediterranean, has alsoproven efficient in restoring degraded estuarine and coastal eco-systems (Piazzi and Ceccherelli 2006).

Moreover, establishment of marine-protected areas or ef-fective fisheries regulations have also been successful in re-covering fish stocks from overfishing (Hutchings andRangeley 2011), but can also catalyze the recovery of ecosys-tems by recovering food web integrity and associated buffers,increasing connectivity and removing physical impacts ofsome fishing practices, such as trawling (Gaines et al. 2010).The benefits of individual marine-protected areas can be fur-ther enhanced by building networks of protected areas which,if properly designed in terms of size, spacing, location, andconfiguration, may also reduce or eliminate the tradeoffbetween achieving conservation and fishery goals(Gaines et al. 2010).

Manipulations of the physical and chemical conditions ofdegraded coastal and estuarine environments to catalyze recov-ery include the use of aeration devices to increase oxygenconcentration (e.g., McLusky and Elliott 2004; Conley 2012)and avoid phosphate release from anoxic sediments (e.g.,Conley et al. 2009); use of gates, dykes, or dredging to increaseflushing and restore the salinity of the ecosystem (e.g., Petersenet al. 2008); and the use of barriers (Greening et al. 2011) orsandbags or fibertex to reduce wave action and sediment resus-pension (Fischer 2011). Deployment of rocks or other settlingstructures, such as seagrass mimics (e.g., Cardoso et al. 2007),has also been used to facilitate the establishment of benthiccommunities (e.g., the EU Life project “Blue Reef” carried outin Denmark). A mimic of rockpool habitats on natural rockyshores has been experimented in seawalls, creating shadedvertical substratum and pools that retain water during low tideand increase diversity of foliose algae and sessile and mobileanimals, especially higher on the shore (e.g., Chapman andUnderwood 2011).

The effectiveness of restoration efforts is rarely evaluated(Benayas et al. 2009). A meta-analysis of restoration effortsconcluded that restoration helped recover biodiversity andecosystem services by, on average, 44 and 25 %, respectively,but rarely achieved recovery back to the baseline (Benayaset al. 2009). Cost–benefit analyses should be used to decideamong the alternative restoration strategies to be deployed inorder to maximize the return on investment on restoration(Benayas et al. 2009), keeping in mind that the evaluation ofbenefits is often more cumbersome than that of costs.

Through these series of actions, ecosystem restoration canachieve a number of goals, such as accelerate recovery, reducehysteresis and time lags, remove buffers precluding recovery,and drive the recovery trajectory towards desired outcomesand stable states.

Towards a Conceptual Model of the Recovery of Coastaland Estuarine Ecosystems

The elements identified in the preceding sections can bearticulated in a conceptual model of the recovery processguiding management and policy actions to improve the statusof degraded coastal and estuarine ecosystems. A general mod-el of the degradation and recovery of coastal and estuarineecosystems acknowledges that the trajectories of degradationand recovery are not parallel, but display hysteresis, and thatthe threshold of pressures conducive to degradation orallowing recovery often differ (Table 2; Fig. 3). The pressurecausing the degradation often needs be reduced much more toallow recovery than to cause degradation, implying that thethreshold of recovery is often set at a much lower level of thepressure than the threshold conducive to degradation, as eco-system buffers and feedback effects, such as resuspension of

Estuaries and Coasts

sediments devoid of vegetation, act to maintain the degradedstate (e.g., Duarte et al. 2009; Steckbauer et al. 2011). Aprerequisite for recovery to be initiated is that the pressuresresponsible for degradation be reduced below the thresholdfor recovery (Figs. 2 and 3). Restoration can catalyze recoveryand/or help the ecosystem achieve a status closer to thepredisturbance state. As restoration acts by removing or re-ducing the negative buffers, it may also affect the location ofthe recovery threshold, thereby lowering the demand for re-duction of the pressures (Figs. 2 and 3).

One important caveat in this conceptual model is that therecovery of coastal and estuarine ecosystems takes place in acontext of global change, where drivers of ecological processesare shifting over time (i.e., a moving baseline), including atmo-spheric composition, climate change, and pollutant loads,among others (Duarte et al. 2009). As a result, the baselinetowards which ecosystems recover following perturbations isconstantly shifting, further amplifying hysteresis, and the timescale to achieve recovery, and confounding the assessment ofrecovery, as the state to what ecosystems recover is not neces-sarily that they displayed before perturbation occurred (Duarteet al. 2009). Moreover, the drift of coastal ecosystems baselineswith global change may render recovery trajectories and targetsless predictable and, as a consequence, more idiosyncratic inthe future, as past states cannot be used to confidently predictrecovery targets (Carstensen et al. 2011).

Overall, the review provided here highlights a need for morecareful definition of recovery targets as well as methods andmetrics needed to assess the course of recovery in specificecosystems. The exploration of recovery paradigms established

that (1) partial recovery prevails, (2) degradation and recoverytypically follow different pathways as buffers act to maintainthe degraded state, and (3) recovery trajectories depend on thenature of the pressure as well as the connectivity of ecosystemsand can differ among ecosystem components and among eco-systems. These paradigms are contained in the conceptualmodel, which also illustrates how restoration efforts may cata-lyze recovery (Figs. 2 and 3). The paradigms can also be used toguide restoration efforts, as restoration efforts directed at in-creasing connectivity or directly initiating populations (e.g.,seagrass restoration projects) and at reducing thresholds forrecovery (e.g., biogeochemical manipulations to revert hypox-ia) should be most effective in catalyzing recovery. The con-ceptual model provided can be used as a basis to formulatenumerical models to test recovery and restoration scenarios forspecific ecosystems.

Acknowledgments This paper is a result of the project WISER (Waterbodies in Europe: Integrative Systems to assess Ecological status andRecovery, www.wiser.eu) funded by the European Union under the 7thFramework Programme, Theme 6 (Environment including ClimateChange) (contract no. 226273) and the Baltic Nest Institute (www.balticnest.org).

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Eco

syst

em s

tate

Time

A

B

C

Degradation Timelag, hysteresis

T1: Release of pressure

Recovery

T0: Increase of pressure

+ Restoration

No restoration

Fig. 3 Schematic illustration of an increase in pressure shifting theecosystem state from a pre-disturbance state (A) to a degraded state (B)(degradation phase, red), and a subsequent release of pressure reflected inan initial “lag/hysteresis phase”where buffers maintain the degraded statefollowed by a “recovery phase” (green) which, over time, leads to therecovered state (C).Gray lines illustrate the recovery phase for a situationwhere restoration efforts are applied to facilitate recovery (+ Restoration)as opposed to a situation without such initiatives (No restoration). Theidentified paradigms (Table 2) refer to the recovery phase

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