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A systematic review of ecological attributes that confer resilience to climate change in environmental restoration

  • Britta L. Timpane-Padgham ,

    britta.timpane-padgham@noaa.gov

    Affiliations School for Marine and Environmental Affairs, University of Washington, Seattle, Washington, United States of America, Ocean Associates Inc., under contract to Northwest Fisheries Science Center, National Marine Fisheries Services, National Oceanic and Atmospheric Association, Seattle, Washington, United States of America

  • Tim Beechie ,

    Contributed equally to this work with: Tim Beechie, Terrie Klinger

    Affiliation Fish Ecology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Association, Seattle, Washington, United States of America

  • Terrie Klinger

    Contributed equally to this work with: Tim Beechie, Terrie Klinger

    Affiliation School for Marine and Environmental Affairs, University of Washington, Seattle, Washington, United States of America

A systematic review of ecological attributes that confer resilience to climate change in environmental restoration

  • Britta L. Timpane-Padgham, 
  • Tim Beechie, 
  • Terrie Klinger
PLOS
x

Abstract

Ecological restoration is widely practiced as a means of rehabilitating ecosystems and habitats that have been degraded or impaired through human use or other causes. Restoration practices now are confronted by climate change, which has the potential to influence long-term restoration outcomes. Concepts and attributes from the resilience literature can help improve restoration and monitoring efforts under changing climate conditions. We systematically examined the published literature on ecological resilience to identify biological, chemical, and physical attributes that confer resilience to climate change. We identified 45 attributes explicitly related to climate change and classified them as individual- (9), population- (6), community- (7), ecosystem- (7), or process-level attributes (16). Individual studies defined resilience as resistance to change or recovery from disturbance, and only a few studies explicitly included both concepts in their definition of resilience. We found that individual and population attributes generally are suited to species- or habitat-specific restoration actions and applicable at the population scale. Community attributes are better suited to habitat-specific restoration at the site scale, or system-wide restoration at the ecosystem scale. Ecosystem and process attributes vary considerably in their type and applicability. We summarize these relationships in a decision support table and provide three example applications to illustrate how these classifications can be used to prioritize climate change resilience attributes for specific restoration actions. We suggest that (1) including resilience as an explicit planning objective could increase the success of restoration projects, (2) considering the ecological context and focal scale of a restoration action is essential in choosing appropriate resilience attributes, and (3) certain ecological attributes, such as diversity and connectivity, are more commonly considered to confer resilience because they apply to a wide variety of species and ecosystems. We propose that identifying sources of ecological resilience is a critical step in restoring ecosystems in a changing climate.

Introduction

Substantial degradation of earth’s ecosystems—and powerful legal mandates such as the U.S. Endangered Species Act, U.S. Clean Water Act, E.U. Water Framework Directive, and E.U. Habitats Directive—have led many governmental agencies, non-profit organizations, and private interest groups to invest in restoration efforts. This ‘restoration economy’ was recently estimated to contribute $24.86 billion and 221,000 jobs annually to the U.S. economy [1]. Yet despite such monumental investments, ecological restoration has often been unsuccessful in reducing extinction rates and slowing declines in habitat quality [25]. On the other hand, evidence of increased biodiversity and improved ecosystem function following restoration demonstrates that restoration can be successful in rehabilitating the condition of ecosystems [5, 6], and restoration now serves as an accepted and widely practiced management action.

Ecological restoration proceeds in the face of advancing climate change, which imposes additional stress on systems already under pressure from human use and this can undermine the long-term success of restoration efforts [7]. To address this concern, many have suggested a shift away from static restoration end points and towards dynamic and adaptive ecological process goals [3, 8, 9]. Evidence suggests that climate change impacts on populations and communities are increasingly considered in the development of management priorities and adaptation plans. For example, recent climate change studies have utilized trait-based vulnerability assessments to identify both potential impacts and inherent natural sources of climate-change resilience for individual species [1014]. These assessments have in turn informed the development of decision-support frameworks to incorporate climate change into restoration planning [15, 16].

Integrating resilience concepts and attributes could help improve restoration and monitoring efforts under conditions of climate change. Resilience approaches to restoration can foster adaptation to future climate impacts [15, 1719] by restoring dynamic processes that promote natural variability and biodiversity within ecological systems, and reducing the risk of dramatic ecosystem change, sharp declines in populations, or loss of ecosystem services [2022]. Ecological resilience incorporates concepts of dynamic feedbacks, unpredictable change, and variation [23, 24]. Here we use the resilience perspective of Walker et al. [25] that defines resilience as the capacity of a system to absorb disturbance and reorganize in ways that retain essentially the same functions, structures, identities, and feedbacks. This definition includes two important mechanisms of resilience, namely resistance to change and recovery from change.

To understand how resilience attributes can be integrated into restoration practices under climate change, we first distilled common attributes of ecological resilience from the published literature. We then applied a ‘climate filter’ to identify attributes likely to confer resilience under changing climate conditions. We further classified these attributes according to their ecological scale of application. We provide three examples to illustrate how practitioners can select resilience attributes that are appropriate for specific management applications. Finally, we outline general strategies for integrating resilience into restoration planning and monitoring in a changing climate.

Methods

Literature selection and examination

We examined the scientific literature to extract attributes of species or ecosystems that have been reported to confer ecological resilience. Using Web of Knowledge, one of us (BLTP) searched using the following terms: (river* OR stream OR (wetland NOT in title) OR ecosystem OR environment*) AND (restor* OR recov* OR re-creat* OR rehabilitat*) AND (resilienc* OR “ecological integrity”), restricting our search to papers published from 2009–2013. From a total of 915 search results, 232 articles were selected for further examination if the title described a scientific study investigating the resilience of some ecological characteristic(s). Of the 232 articles, 111 were selected for full review based on relevance to the study objectives as inferred from the abstract. Fifty-nine additional articles were gleaned from the selected literature based on best professional judgment of their fit with the goals of this study. These articles were added to the analysis for a total of 170 articles examined in this study (S1 Fig). For consistency, and to reduce inter-observer variation, all examination of the literature was performed by BLTP.

Resilience attribute identification

Attributes of ecological resilience were selected for further consideration if they were (1) typical of more than one ecosystem or species, (2) distinct from other attributes, and (3) measureable. From the assembled attributes, we created a database in which every attribute from each publication was recorded, along with the source of publication, ecosystem context, metric(s) used to measure or monitor the attribute, and whether the attribute was identified as conferring resistance to or recovery from disturbance. We then grouped the attributes into major categories and combined attributes that were similar to produce a list of 51 resilience attributes classified into five major categories. The resilience attributes that we identified come from a wide-range of ecosystems and range from more general (e.g. energy flows) to more specific (e.g. soil and air carbon balance). Given that our primary purpose in this study was to broadly inform restoration practices under climate change, we elected to retain as many attributes as possible and to broadly define terms to maximize utility to practitioners working across a range of scales and contexts. Practitioners can choose to further refine attributes and definitions based on specific applications.

Climate change filter

We next evaluated the attributes to identify those that were considered to confer resilience to climate change. An attribute passed through the climate change filter if the article specifically mentioned an attribute in relation to climate change or climate impacts. For example, if the article discussed how an attribute might confer resilience to climate change or an ecological feature directly affected by climate change such as stream flow or temperature, the attribute was retained in our list of resilience attributes. A total of 45 (out of 51) attributes remained after the climate filter was applied. Attributes eliminated by the climate filter (population (beta) diversity, gamma diversity, food-web complexity, large woody debris, salinity, and historical flow-disturbance regimes) may confer resilience to climate change impacts in some situations, but that was not apparent in the articles evaluated.

Attribute classification

We classified the 45 resilience attributes from our review into five categories that roughly equate to ecological scale: (1) individual attributes, (2) population attributes, (3) community attributes, (4) ecosystem attributes, and (5) process attributes. We used best professional judgment to classify each attribute by two criteria that we felt were integral for any restoration project: restoration focus (e.g., is the restoration effort species-specific, habitat-specific, or system-wide focused?) and scale of application (e.g., do restoration actions take place at a population, site, or ecosystem scale?). ‘Restoration focus’ refers to the type of project an attribute is best suited for. For example, a population attribute such as density is likely more suitable for a restoration effort that aims to restore a species, whereas a community attribute such as functional diversity is more applicable to a restoration effort aiming to restore an ecosystem. Some attributes were assigned to more than one category because they are suitable for more than one restoration focus. ‘Scale of Application’ denotes the scale an attribute can be used to describe (e.g., generally population scales for biological attributes, and site or ecosystem scales for environmental attributes). Several attributes were assigned to more than one scale because scale varies depending on environmental context or project type. Our classification does not account for every potential application; consequently, users may need to tune some classifications to meet the needs of particular systems or projects.

In a practical sense, the resilience attributes all serve as ecological metrics that can be used for monitoring efforts (e.g. population size, presence of propagules, recovery time after disturbance) and/or setting ecological goals for restoration projects (e.g. genetic diversity, increase or establish refugia or support areas, release from competition or predation).

Attribute selection and sample applications

The attribute classifications can be used to create a decision support table (DST) by using a filtering function (S1 Table) so that practitioners can identify resilience attributes that are best suited to the focus and spatial scale of a specific restoration plan or project. To create a sub-list of suitable resilience attributes, a practitioner can sort attributes by asking: (1) what is the focus of the restoration project? and (2) what is the spatial scale of the specific needs? The output comprises a sub-set of resilience attributes that are more likely to be relevant to the specific plan or project.

To illustrate use of the DST in restoration planning, we created three sample applications. We selected three different restoration efforts focused at different spatial scales to demonstrate (1) how relevant resilience attributes can be identified for a specific project and (2) how the attributes selected will differ according to the type of project. We use the Kissimmee watershed system as an example of restoration at the ecosystem scale, a Pacific salmon (Oncorhynchus spp.) population as an example of restoration at the population scale, and vulnerable coral species as an example of restoration at the site scale.

Results and discussion

Summary of literature examined

Most articles referred to riverine and coral ecosystems (32 and 28 citations, respectively), followed by terrestrial, marine, and forest ecosystems (Fig 1). Rocky shore, wetland, and grassland ecosystems were less commonly cited (4 citations each). While our search terms did include river or stream habitats, as that was our intended focus originally, we also include broader terms of ‘ecosystem’ or ‘environment’ which resulted in a diverse representation of habitat types. The number of times an individual attribute was cited varied from 1–20. By attribute type, ecosystem attributes were most frequently cited (Table 1), but there were more total citations of process attributes (63) because more than one third of all attributes (16, or 36%) were classified as process attributes.

More than half (33 of 45) of the resilience attributes were defined as equivalent to resistance (to perturbation), and many others (42 of 45) used resilience synonymously with recovery, or as an outcome of recovery (Table 1). Across all studies, 30 of the 45 attributes were used in both ways (i.e., some studies considered resilience to mean recovery, while others considered it to mean resistance). However, only a few sources explicitly considered resilience to include both concepts: that of resistance, or the ability of an ecosystem or community to persist through a disturbance, and that of recovery, or rate at which a system or community returns to its functional state.

Several studies in our review consisted of a census of resilience attributes within a specific ecosystem type [15, 51, 54, 58, 66, 113, 126]. Maynard et al. [66] used a literature review to distill a list of 19 ‘resilience indicators’ that ‘conferred resilience’ within coral reef systems. In a study by McClanahan et al. [113], a group of 50 scientists ranked and scored an existing list of ‘resilience factors’ also in coral reef systems. Bernhardt and Leslie [126] conducted a comprehensive study exploring sources of resilience to climate change within coastal marine ecosystems and found three important ecological themes for conferring resilience: connectivity, biological diversity, and adaptability. Our review, which included the aforementioned studies, also found these three ecological themes to be widely cited in the literature, but to these we add habitat variability and condition, presence of refugia or support areas, and natural disturbance history as commonly-cited themes. We discuss these themes and the influence of human pressures on resilience in the following sections.

Connectivity

Connectivity was found to enhance capacity for self-organization and recovery at multiple scales, including interactions between species at community and population scales and connectivity of habitat types and ecosystems throughout both space and time [126]. Connectivity supports resilience by allowing movement of propagules, larvae and adults to recolonize a disturbed area or replenish an area with new genetic material and enhance local populations. Fritz and Dodds [42] observed how flooding events increasing invertebrate populations by connect intermittent pools in rivers and provided for colonization and dispersed young individuals. In coral reef systems, Olds et al. [78] found that connectivity between mangrove ecosystems and protected reefs in eastern Australia enhanced herbivore biomass and richness.

Connectivity of various healthy habitat types helps maintain species that use a variety of habitats for feeding, reproduction, resting, rearing, refuge, and migrating [51]. In riverine systems, ecological connectivity is important for maintaining natural variability and supporting productivity [102]. Many species, such as Pacific salmon, rely on movement throughout the system, including the mainstem, tributaries, floodplain habitats, and deltas. Removal of anthropogenic barriers to migration can help increase resilience of aquatic biota to climate change impacts such as changing flow regimes [151]. Ecosystem connectivity is also critical to help regulate essential abiotic and biotic processes such as flow, temperature, water quality, aquatic and terrestrial interactions and food webs.

Biodiversity and the insurance hypothesis

Alpha diversity, genetic diversity, and functional diversity were the most frequently cited diversity attributes. Duffy [154] found that on average, greater species richness increased resource use within trophic levels and accumulation of biomass, and that the variance in these responses was reduced over time. Moreover, diverse communities have a higher chance of including either disturbance-resistant species or species that are able to recover quickly from a variety of perturbations [126, 176]. Ecosystems or communities with greater functional and response diversity are able to maintain important ecosystem processes that sustain function and result in ‘no net loss’ in productivity, often referred to as the insurance hypothesis [94, 116, 147, 164]. In an experimental study Naeem and Li [147] tested the hypothesis that a greater number of species should enhance the probability that a system will provide a more “consistent level of performance” using microbes. They found that the greater number of species per functional group led to more consistent biomass and density measures within the replicated microbial microcosms. Genetic diversity can provide this benefit by increasing the critical response diversity among populations and can help maintain ecosystem function [112, 126]. Additionally, increased genetic diversity has been shown to promote population growth and improve fitness [177].

There is ongoing debate over the association between biodiversity and its influence on resilience. Not all findings support the insurance hypothesis. For example, in a greenhouse experiment, Lanta et al. [57] found that high species richness and functional diversity provided less resistance against drought stressed conditions than less diverse species assemblages. The same study found no effect of diversity on community resistance under outdoor experimental conditions. Similarly, in a study examining species richness in aquatic food webs, Downing and Leibold [63] found that while respiration rates showed “higher resilience” in species-rich communities, they did not exhibit increased “resistance” to disturbance. In contrast, however, a number of studies have found strong causal linkages between diversity measurements and productivity or stability in a number of terrestrial and aquatic systems [154], including seagrass [130, 136] and forests [38, 178].

Habitat variability and condition

Spatial and temporal variability in habitats have been observed to maintain higher levels of biodiversity [94], and thus contribute to ecosystem resilience. A study conducted by Oliver and others [64] found landscape structure, including increased heterogeneity within habitat patches, to influence resilience of populations to extreme climatic events. A landscape with a more heterogeneous habitat structure was more likely to contain refuge microclimates to support survival of the ringlet butterfly, and greater heterogeneity among habitat patches increased the likelihood of harboring species more resilient to extreme events [64]. Within river systems, spatiotemporal variability in flow and temperature regimes was found to regulate suitable habitat and maintain flexible species adaptations [58, 67, 79]. Milner et al. [151] showed that maintaining habitat heterogeneity can maximize resilience of aquatic species to altered flow regimes associated with climate change. While habitat variability generally increases diversity at various scales, it also serves as a useful “measure of resilience to impending climate change” [165].

Refugia and support areas

Within the ecosystem category, presence of refugia or support areas was particularly important to ecosystem resilience. In freshwater and salt marsh ecosystems, presence and type of riparian vegetation was found to create micro-habitats that promoted community resistance to dry conditions [35, 62, 80]. Various soil health metrics were identified as crucial for aiding in recovery of forest ecosystems [107, 132] and improving functional resilience in other terrestrial ecosystems [179181]. Studies in coral reef systems identified water quality to be an important control on macroalgal growth, which can cause serious negative impacts to coral recruitment and overall reef resilience [59, 78, 135]. Refugia can also serve as areas where species are able to survive or rest from disturbance [19, 29, 55, 67, 68, 79, 82, 141], and have been documented to provide propagules or seed sources for recovery in other affected areas [26, 28, 37, 151, 182]. These particular habitat attributes may not influence resilience in every ecosystem, but these findings suggest that identifying principal habitat characteristics may be an important consideration in monitoring resilience within an ecosystem.

Natural disturbance history and adaptability

A history of natural environmental fluctuations and disturbance is one process that maintains habitat heterogeneity, and the variability induced by disturbances favors biodiversity [94]. Specifically, disturbance can regulate habitat structure at multiple scales, with the potential to affect species richness many years into the future [52, 83, 86, 107]. A substantial proportion of the literature identified presence of natural disturbance as an important determinant for recovery rates, creation of alternate trajectories, and building biological capacity to adapt to or resist change. Systems that are naturally subjected to a variety of disturbances contain biota that have evolved life history traits favoring adaptability or flexibility [61, 114, 182]. Li et al. [61] determined that bacterioplankton communities in a lake ecosystem had developed a number of life history attributes (e.g., high growth rates, phenotypic flexibility) that favored adaptation and explained their high resilience to natural pulses of Microcystis blooms. Within marine ecosystems, Neubauer et al. [45] confirmed that a history of moderate exploitation within fisheries populations can increase their rate of recovery.

Natural disturbance can influence biophysical characteristics of ecosystems and populations. For example, the size of a disturbed area can influence recovery rates because it effects how close it is to undisturbed neighboring areas that can provide material for re-colonization [162]. Some authors characterized entire ecosystems that are subject to high levels of natural disturbance as resilient. The hypothesis is that systems with high levels of disturbance have adapted with species and or processes that support quick recovery or resist complete change altogether [7, 19, 75, 83, 90, 182, 183]. In addition to disturbance, the magnitude and duration of an event proved to be an important attribute conferring resilience within many different systems. A number of studies found disturbance intensity to affect the degree of recovery [136, 149] with more severe disturbance being a predictor of more rapid recovery [48, 169]. Despite many systems demonstrating a considerable resilience to disturbance, prolonged disturbance is more likely to result in persistent habitat changes and reduce the ability of a system or populations to recover [175]. There is also considerable concern about future impacts on disturbance duration, magnitude, frequency, and timing from human induced climate change [149, 166].

The effects of increased disturbance due to climate change do pose serious unknowns for resilience. For example, holm oak woodlands are historically highly resilient to fire frequencies of about 50 year intervals, but if the frequency of fire increases in response to climate change the system may not exhibit the same degree of resilience [149]. In a study examining resilience of fishes and invertebrates in streams exposed to prolonged drought, Bêche and others [175] found that both severity and duration of drought disturbance influenced the abundance, richness, and general recovery of aquatic communities.

Human pressures, cumulative effects

We found contradictory evidence regarding the effects of human pressures on resilience. A number of studies reported that isolation from human pressures or reduced exposure to anthropogenic stressors increased resilience within their systems [33, 121, 133]. Alternatively, in a study of coral assemblages distributed over a wide geographic range, Côté and Darling [54] found that if there is a positive co-tolerance between non-climatic disturbance and climatic impacts among coral species, then some degree of human-caused degradation may “increase the abundance of disturbance-tolerant species within a community and thus the ability of an ecosystem to resist impacts of climatic disturbance”. However, reduced abundance of less tolerant species (and increased proportions of disturbance-tolerant species) can also be considered an indicator of ecosystem degradation, at least in some contexts [184].

A number of resilience attributes we identified, including exposure to human pressures, were often discussed in context of cumulative impacts. This is an important consideration when measuring resilience in locations subject to multiple human stressors. The ability of ecosystems and their components to maintain resilience in the face of climate change when those systems are already under stress from cumulative human-generated impacts is a topic of evident concern in the literature [3, 54, 159]. Multiple co-occurring modes of disturbance can confound efforts to identify, measure, and monitor resilience within a system.

Restoration examples using the DST

Attributes classified by restoration focus and scale of measurement roughly sorted according to attribute category (Table 2). For example, individual and population attributes (e.g., dispersal potential or genetic diversity) tended to be associated with species-specific restoration actions and with resilience at the population scale. Community attributes generally described the structure and diversity of ecosystems (e.g., community structure, functional diversity, or species diversity), and therefore were most often associated with site-specific or system-wide restoration. Roughly half of the ecosystem attributes (e.g., habitat area and condition, or refuge areas) were associated with all three restoration foci and at all three spatial scales. Process attributes were most diverse with respect to both focus and scale.

We illustrate how resilience metrics might be used in conservation or management of species or ecosystems with three applied examples. In each example, we focus on how practitioners might select a sub-set of resilience attributes for characterizing or monitoring resilience of species or ecosystems using the DST. The examples we selected—restoration of the Kissimmee River system in Florida, recovery of an endangered salmon population, and coral species restoration—demonstrate how a sub-set of resilience attributes and metrics differ depending on biological and management contexts and the scale at which attributes are measured.

Restoration at the ecosystem scale–the Kissimmee River example.

The Kissimmee River once meandered for more than 100 miles through central Florida; connecting diverse habitats and supporting a thriving wetland ecosystem [185]. Restoration of the Kissimmee River System in Florida began two decades ago, and aims to reverse channelization and draining of wetlands to restore floodplain connectivity and restore ecosystem processes important to both the Kissimmee River and the Everglades ecosystem to which it drains. Based on the restoration focus (system) and scale (ecosystem) of the restoration effort, we derived 23 resilience attributes from the DST (Table 2) that are appropriate as restoration or monitoring variables. These attributes represent the community, ecosystem, and process categories (Table 3). Key resilience attributes within the community category are assemblage, diversity, redundancy, and connectivity. Not surprisingly, resilience attributes related to connectivity appear in all three major categories, as connectivity is a cornerstone of efforts to restore the Kissimmee River and Everglades ecosystem. In this case, each connectivity attribute increases resilience by allowing organisms and materials to move freely as suitable habitats shift in location. Within the ecosystem category, habitat area, condition, and variability are attributes that can support diversity or redundancy. Restoration efforts have largely focused on increasing natural habitat area and condition, including water quality and flow which are key metrics used to evaluate restoration success [185]. The remaining attributes in the process category tend to be features that also influence habitat condition and therefore support the community attributes. For example, energy flows is a broad and somewhat non-descript metric, however in this ecological context managers or restoration practitioners could consider (and already are) measuring how much water, sediment, and/or nutrients move between refuge areas.

Restoration at the population scale–the pacific salmon Example.

Recovery of salmon populations listed under the Endangered Species Act focuses on achieving several important targets, including adequate population size, population growth rate, spatial distribution, and diversity [186]. Each of these targets are listed in the resilience attributes’ population category and they are monitored and population performance is assessed using these criteria every 5 years. That is, these resilience attributes were selected to characterize recovery of salmon populations in part because they indicate both recovery of number of fish and recovery of population attributes that buffer populations against environmental change. This comports well with our DST, which suggests that relevant resilience attributes include genetic diversity and connectivity as well as growth, size, abundance, and life history flexibility in individuals and populations (Table 4). In addition, delisting criteria consider whether habitat factors contributing to listing have been abated. Consequently, various habitat-related resilience attributes are also appropriate for consideration in restoration planning or monitoring recovery. Habitat characteristics such as area, condition, and presence of refugia play an important role in the restoration of endangered populations and are often key components for the recovery of any species listed under the ESA. In addition to the metrics that align with current actions regarding salmon restoration, the DST provides several novel metrics that could be used to increase the resilience of endangered salmon populations to climate change, or to monitor changes in resilience among salmon populations.

Restoration at the site scale–the coral reef example.

One common management strategy for coral reef protection and restoration is the creation of Marine Protected Areas (MPA’s) [187]. For example, the Coral Triangle Initiative, a multi-lateral effort to address threats to reefs, fisheries, and food security in the South Pacific, is working towards establishing regional connectivity between MPA’s [188]. Restoration activities that focus on specific sites or habitats are more common for sessile species where the focus is either on restoring habitat for a species or ‘seeding’ a species to initiate recovery at a site and many of the following attributes resulting from the DST depend on having available habitat. Individual, ecosystem, and process categories are represented in the list of suitable resilience attributes for this type of restoration (Table 5). Individual attributes speak to a species’ ability to persist in an area. Ecosystem attributes are focused on habitat characteristics that may affect a species such as its condition, structure, or whether there are support areas present. Key process attributes that may affect habitat or species include structural legacies, disturbance, or degree of exposure to human pressures. Evidence suggests that conservation of sessile organisms such as coral reefs is most effective when an Ecosystem-based Management approach is taken. To address the many threats to coral reefs the creation of an MPA is coupled with land-based management to help reduce pollution sources [189].

Resilient restoration

Explicit consideration of climate change in restoration design is an increasingly common request among federal and state governmental agencies [15, 16, 190, 191], and many restoration projects are now required to evaluate the ability of a restored system or site to withstand impacts from climate change. Evidence suggests that when resilience is made an explicit planning objective, it offers a way to improve restoration projects as a whole [51, 102].

The purpose of our analysis is to assist restoration practitioners in identifying appropriate resilience attributes to measure and monitor within particular systems. The focus of the management or restoration action (species, habitat, or system) is the first basis for categorizing the resilience attributes, because the overarching goal or motivation of restoration will dictate objective setting and monitoring design. The scale at which the attributes should be measured is the second basis for selecting attributes. Together these two criteria can help distill a subset of potential resilience attributes that are suitable for a specific restoration action or monitoring efforts. The attributes and their associated metrics should be part of an adaptive management framework to be evaluated for their usefulness in conferring resilience to climate change.

Conclusion

From our examination of recent ecological literature, we have extracted three key points that may be helpful in integrating resilience metrics into restoration plans. First, if made an explicit planning objective, as opposed to a component of existing objectives, resilience may be a way to improve restoration projects as a whole [51, 102]. By planning and monitoring for resilience, we are forced to identify sources of adaptive capacity within restored and natural ecosystems and to define actions that foster resilience. Second, considering the restoration focus and scale of a plan or project is essential in choosing appropriate resilience metrics to inform restoration efforts. In the face of climate change, restoration approaches that promote natural sources of resilience are more likely to be successful than those that focus on creating optimal steady states. Third, certain ecological attributes, such as diversity and connectivity, are more commonly considered to confer resilience because they apply to a wide variety of species and ecosystems. Even so, we identified numerous additional metrics that could potentially be useful for resilience planning.

The need to understand the dynamic nature of ecological systems, especially in the context of climate change, is crucial for successful restoration work. Improving our understanding of how certain ecological attributes confer resilience will help practitioners develop best practices for successful restoration in a changing climate. Past trends in climate and streamflow, for example, make it clear that stationarity of the physical environment is no longer a valid assumption in restoration planning. Moreover, we should not assume continuous directional change in ecosystems, as climate cycles and other sources of natural variability drive annual or decadal variation in habitats and species. Hence, assumptions made about response and recovery trajectories can greatly influence restoration planning decisions. By monitoring the response and recovery of a variety of species and ecosystems, we can better understand which attributes most contribute to ecological resilience to climate change.

Supporting information

S1 Table. Interactive decision support table (DST).

https://doi.org/10.1371/journal.pone.0173812.s002

(XLSX)

Acknowledgments

We thank Sarah Morley, George Pess and Lara Hansen for helpful reviews of the manuscript.

Author Contributions

  1. Conceptualization: BLTP TB TK.
  2. Data curation: BLTP.
  3. Formal analysis: BLTP.
  4. Investigation: BLTP.
  5. Methodology: BLTP TB TK.
  6. Project administration: BLTP TK.
  7. Supervision: TB TK.
  8. Validation: BLTP.
  9. Visualization: BLTP.
  10. Writing – original draft: BLTP.
  11. Writing – review & editing: BLTP TB TK.

References

  1. 1. BenDor T, Lester TW, Livengood A, Davis A, Yonavjak L. Estimating the Size and Impact of the Ecological Restoration Economy. PLoS One. 2015;10(6):e0128339. pmid:26083034
  2. 2. Bernhardt ES, Palmer M, Allan J, Alexander G, Barnas K, Brooks S, et al. Synthesizing US river restoration efforts. Science. 2005;308(5722):636–7. pmid:15860611
  3. 3. Palmer M, Bernhardt E, Allan J, Lake P, Alexander G, Brooks S, et al. Standards for ecologically successful river restoration. Journal of applied ecology. 2005;42(2):208–17.
  4. 4. Norton DA. Species invasions and the limits to restoration: learning from the New Zealand experience. Science. 2009;325(5940):569–71. pmid:19644109
  5. 5. Benayas JMR, Newton AC, Diaz A, Bullock JM. Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. science. 2009;325(5944):1121–4. pmid:19644076
  6. 6. Bullock JM, Aronson J, Newton AC, Pywell RF, Rey-Benayas JM. Restoration of ecosystem services and biodiversity: conflicts and opportunities. Trends in Ecology & Evolution. 2011;26(10):541–9.
  7. 7. Palmer MA, Reidy Liermann CA, Nilsson C, Flörke M, Alcamo J, Lake PS, et al. Climate change and the world's river basins: anticipating management options. Frontiers in Ecology and the Environment. 2008;6(2):81–9.
  8. 8. Choi YD. Theories for ecological restoration in changing environment: toward ‘futuristic’restoration. Ecological Research. 2004;19(1):75–81.
  9. 9. Lawler JJ. Climate change adaptation strategies for resource management and conservation planning. Annals of the New York Academy of Sciences. 2009;1162(1):79–98.
  10. 10. Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G. Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol. 2008;6(12):e325.
  11. 11. Glick P, Stein B, Edelson N. Scanning the conservation horizon: a guide to climate change vulnerability assessment. Washington (DC): National Wildlife Federation. 2011.
  12. 12. Foden WB, Butchart SH, Stuart SN, Vié J-C, Akçakaya HR, Angulo A, et al. Identifying the world's most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS One. 2013;8(6):e65427. pmid:23950785
  13. 13. Morrison WE, Nelson MW, Howard JF, Teeters EJ, Hare JA, Griffis RB, et al. Methodology for Assessing the Vulnerability of Marine Fish and Shellfish Species to a Changing Climate. In: Commerce USDo, editor.: NOAA Technical Memorandum; 2015. p. 48 p.
  14. 14. Hare JA, Morrison WE, Nelson MW, Stachura MM, Teeters EJ, Griffis RB, et al. A vulnerability assessment of fish and invertebrates to climate change on the Northeast US Continental Shelf. PloS one. 2016;11(2):e0146756. pmid:26839967
  15. 15. Beechie T, Imaki H, Greene J, Wade A, Wu H, Pess G, et al. Restoring salmon habitat for a changing climate. River Research and Applications. 2013;29(8):939–60.
  16. 16. Perry LG, Reynolds LV, Beechie TJ, Collins MJ, Shafroth PB. Incorporating climate change projections into riparian restoration planning and design. Ecohydrology. 2015;8(5):863–79.
  17. 17. Hansen LJ, Biringer JL, Hoffman J. Buying time: a user’s manual for building resistance and resilience to climate change in natural systems. WWF, Washington. 2003.
  18. 18. Beatley T. Planning for coastal resilience: best practices for calamitous times: Island Press; 2012.
  19. 19. Seavy NE, Gardali T, Golet GH, Griggs FT, Howell CA, Kelsey R, et al. Why climate change makes riparian restoration more important than ever: recommendations for practice and research. Ecological Restoration. 2009;27(3):330–8.
  20. 20. Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, et al. Regime shifts, resilience, and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics. 2004:557–81.
  21. 21. Walker B, Salt D. Resilience thinking: sustaining ecosystems and people in a changing world: Island Press; 2012.
  22. 22. Beechie TJ, Sear DA, Olden JD, Pess GR, Buffington JM, Moir H, et al. Process-based principles for restoring river ecosystems. BioScience. 2010;60(3):209–22.
  23. 23. Holling CS. Engineering resilience versus ecological resilience. Engineering within ecological constraints. 1996:31–44.
  24. 24. Parrish JD, Braun DP, Unnasch RS. Are we conserving what we say we are? Measuring ecological integrity within protected areas. BioScience. 2003;53(9):851–60.
  25. 25. Walker B, Holling CS, Carpenter SR, Kinzig A. Resilience, adaptability and transformability in social—ecological systems. Ecology and society. 2004;9(2):5.
  26. 26. Nyström M, Folke C. Spatial resilience of coral reefs. Ecosystems. 2001;4(5):406–17.
  27. 27. Pollack JB, Kim H-C, Morgan EK, Montagna PA. Role of flood disturbance in natural oyster (Crassostrea virginica) population maintenance in an estuary in South Texas, USA. Estuaries and Coasts. 2011;34(1):187–97.
  28. 28. Chester E, Robson B. Drought refuges, spatial scale and recolonisation by invertebrates in non-perennial streams. Freshwater Biology. 2011;56(10):2094–104.
  29. 29. Baker AC, Glynn PW, Riegl B. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, coastal and shelf science. 2008;80(4):435–71.
  30. 30. Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, et al. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment. 2003;1(9):488–94.
  31. 31. Obura DO. Resilience and climate change: lessons from coral reefs and bleaching in the Western Indian Ocean. Estuarine, Coastal and Shelf Science. 2005;63(3):353–72.
  32. 32. Provan J, Beatty GE, Keating SL, Maggs CA, Savidge G. High dispersal potential has maintained long-term population stability in the North Atlantic copepod Calanus finmarchicus. Proceedings of the Royal Society of London B: Biological Sciences. 2009;276(1655):301–7.
  33. 33. McClanahan T, Polunin N, Done T. Ecological states and the resilience of coral reefs. Conservation ecology. 2002;6(2):18.
  34. 34. Carvalho P, THOMAZ S, Kobayashi JT, BINI L. Species richness increases the resilience of wetland plant communities in a tropical floodplain. Austral Ecology. 2013;38(5):592–8.
  35. 35. Sridhar V, Sansone AL, LaMarche J, Dubin T, Lettenmaier DP. Prediction of stream temperature in forested watersheds. Journal of the American Water Resources Association: Wiley Online Library; 2004. p. 197–213.
  36. 36. Bellwood DR, Hoey AS, Hughes TP. Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proceedings of the Royal Society of London B: Biological Sciences. 2011:rspb20111906.
  37. 37. Kroon F, Ludwig J. Response and recovery of fish and invertebrate assemblages following flooding in five tributaries of a sub-tropical river. Marine and Freshwater Research. 2010;61(1):86–96.
  38. 38. Royer-Tardif S, Bradley R, Parsons W. Evidence that plant diversity and site productivity confer stability to forest floor microbial biomass. Soil Biology and Biochemistry. 2010;42(5):813–21.
  39. 39. Thrush SF, Hewitt JE, Lohrer AM, Chiaroni LD. When small changes matter: the role of cross-scale interactions between habitat and ecological connectivity in recovery. Ecological Applications. 2013;23(1):226–38. pmid:23495648
  40. 40. King EG, Franz TE, Caylor KK. Ecohydrological interactions in a degraded two-phase mosaic dryland: implications for regime shifts, resilience, and restoration. Ecohydrology. 2012;5(6):733–45.
  41. 41. Mori AS, Furukawa T, Sasaki T. Response diversity determines the resilience of ecosystems to environmental change. Biological Reviews. 2013;88(2):349–64. pmid:23217173
  42. 42. Fritz KM, Dodds WK. Resistance and resilience of macroinvertebrate assemblages to drying and flood in a tallgrass prairie stream system. Hydrobiologia. 2004;527(1):99–112.
  43. 43. Pernetta J. Mangrove forests, climate change and sea level rise: hydrological influences on community structure and survival, with examples from the Indo-West Pacific: IUCN; 1993.
  44. 44. Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, et al. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental conservation. 2002;29(04):436–59.
  45. 45. Neubauer P, Jensen OP, Hutchings JA, Baum JK. Resilience and recovery of overexploited marine populations. Science. 2013;340(6130):347–9. pmid:23599493
  46. 46. Koski K. The fate of coho salmon nomads: the story of an estuarine-rearing strategy promoting resilience. Ecology and Society. 2009;14(1):4.
  47. 47. Mumby PJ. The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecological Applications. 2006;16(2):747–69. pmid:16711060
  48. 48. Graham N, Nash K, Kool J. Coral reef recovery dynamics in a changing world. Coral Reefs. 2011;30(2):283–94.
  49. 49. Krosby M, Tewksbury J, Haddad NM, Hoekstra J. Ecological connectivity for a changing climate. Conservation Biology. 2010;24(6):1686–9. pmid:20961330
  50. 50. Suding KN, Gross KL. The dynamic nature of ecological systems: multiple states and restoration trajectories. Foundations of restoration ecology. 2006:190–209.
  51. 51. Thom RM, Diefenderfer HL, Vavrinec J, Borde AB. Restoring resiliency: case studies from Pacific Northwest estuarine eelgrass (Zostera marina L.) ecosystems. Estuaries and Coasts. 2012;35(1):78–91.
  52. 52. Morimoto M, Morimoto J, Moriya Y, Nakamura F. Forest restoration following a windthrow: how legacy retention versus plantation after salvaging alters the trajectory of initial recovery. Landscape and ecological engineering. 2013;9(2):259–70.
  53. 53. Baldwin AH, Platt WJ, Gathen KL, Lessmann JM, Rauch TJ. Hurricane damage and regeneration in fringe mangrove forests of southeast Florida, USA. Journal of Coastal Research. 1995:169–83.
  54. 54. Côté IM, Darling ES. Rethinking ecosystem resilience in the face of climate change. PLoS Biol. 2010;8(7):e1000438. pmid:20668536
  55. 55. Garcia X-F, Schnauder I, Pusch M. Complex hydromorphology of meanders can support benthic invertebrate diversity in rivers. Hydrobiologia. 2012;685(1):49–68.
  56. 56. Altieri AH, Bertness MD, Coverdale TC, Axelman EE, Herrmann NC, Szathmary PL. Feedbacks underlie the resilience of salt marshes and rapid reversal of consumer-driven die-off. Ecology. 2013;94(7):1647–57. pmid:23951724
  57. 57. Lanta V, Doležal J, Zemková L, Lepš J. Communities of different plant diversity respond similarly to drought stress: experimental evidence from field non-weeded and greenhouse conditions. Naturwissenschaften. 2012;99(6):473–82. pmid:22580797
  58. 58. Stromberg J, McCluney K, Dixon M, Meixner T. Dryland riparian ecosystems in the American southwest: sensitivity and resilience to climatic extremes. Ecosystems. 2013:1–5.
  59. 59. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, et al. Climate change, human impacts, and the resilience of coral reefs. science. 2003;301(5635):929–33. pmid:12920289
  60. 60. Speed JD, Cooper EJ, Jónsdóttir IS, Van Der Wal R, Woodin SJ. Plant community properties predict vegetation resilience to herbivore disturbance in the Arctic. Journal of Ecology. 2010;98(5):1002–13.
  61. 61. Li H, Xing P, Wu QL. The high resilience of the bacterioplankton community in the face of a catastrophic disturbance by a heavy Microcystis bloom. FEMS microbiology ecology. 2012;82(1):192–201. pmid:22632738
  62. 62. Stubbington R, Datry T. The macroinvertebrate seedbank promotes community persistence in temporary rivers across climate zones. Freshwater Biology. 2013;58(6):1202–20.
  63. 63. Downing AL, Leibold MA. Species richness facilitates ecosystem resilience in aquatic food webs. Freshwater Biology. 2010;55(10):2123–37.
  64. 64. Oliver TH, Brereton T, Roy DB. Population resilience to an extreme drought is influenced by habitat area and fragmentation in the local landscape. Ecography. 2013;36(5):579–86.
  65. 65. Hilborn R, Quinn TP, Schindler DE, Rogers DE. Biocomplexity and fisheries sustainability. Proceedings of the National Academy of Sciences. 2003;100(11):6564–8.
  66. 66. Maynard J, Marshall P, Johnson J, Harman S. Building resilience into practical conservation: identifying local management responses to global climate change in the southern Great Barrier Reef. Coral Reefs. 2010;29(2):381–91.
  67. 67. Caissie D. The thermal regime of rivers: a review. Freshwater Biology. 2006;51(8):1389–406.
  68. 68. Stubbington R. The hyporheic zone as an invertebrate refuge: a review of variability in space, time, taxa and behaviour. Marine and Freshwater Research. 2012;63(4):293–311.
  69. 69. LOBÓN-CERVIÁ J. Why, when and how do fish populations decline, collapse and recover? The example of brown trout (Salmo trutta) in Rio Chaballos (northwestern Spain). Freshwater Biology. 2009;54(6):1149–62.
  70. 70. Micheli F, Saenz-Arroyo A, Greenley A, Vazquez L, Montes JAE, Rossetto M, et al. Evidence that marine reserves enhance resilience to climatic impacts. PloS one. 2012;7(7):e40832. pmid:22855690
  71. 71. Magalhães WF, Barros F. Structural and functional approaches to describe polychaete assemblages: ecological implications for estuarine ecosystems. Marine and Freshwater Research. 2011;62(8):918–26.
  72. 72. Schneck F, Melo AS. Hydrological disturbance overrides the effect of substratum roughness on the resistance and resilience of stream benthic algae. Freshwater Biology. 2012;57(8):1678–88.
  73. 73. Nuñez TA, Lawler JJ, Mcrae BH, PIERCE D, Krosby MB, Kavanagh DM, et al. Connectivity planning to address climate change. Conservation Biology. 2013;27(2):407–16. pmid:23410037
  74. 74. Churchill DJ, Larson AJ, Dahlgreen MC, Franklin JF, Hessburg PF, Lutz JA. Restoring forest resilience: from reference spatial patterns to silvicultural prescriptions and monitoring. Forest Ecology and Management. 2013;291:442–57.
  75. 75. Niemi GJ, DeVore P, Detenbeck N, Taylor D, Lima A, Pastor J, et al. Overview of case studies on recovery of aquatic systems from disturbance. Environmental management. 1990;14(5):571–87.
  76. 76. Hodgson JA, Moilanen A, Wintle BA, Thomas CD. Habitat area, quality and connectivity: striking the balance for efficient conservation. Journal of Applied Ecology. 2011;48(1):148–52.
  77. 77. Brauman KA, Daily GC, Duarte TKe, Mooney HA. The nature and value of ecosystem services: an overview highlighting hydrologic services. Annu Rev Environ Resour. 2007;32:67–98.
  78. 78. Olds AD, Pitt KA, Maxwell PS, Connolly RM. Synergistic effects of reserves and connectivity on ecological resilience. Journal of Applied Ecology. 2012;49(6):1195–203.
  79. 79. Chu C, Jones NE, Mandrak NE, Piggott AR, Minns CK. The influence of air temperature, groundwater discharge, and climate change on the thermal diversity of stream fishes in southern Ontario watersheds. canadian Journal of Fisheries and aquatic sciences. 2008;65(2):297–308.
  80. 80. D'Alpaos A. The mutual influence of biotic and abiotic components on the long-term ecomorphodynamic evolution of salt-marsh ecosystems. Geomorphology. 2011;126(3):269–78.
  81. 81. Grimsditch GD, Salm RV. Coral reef resilience and resistance to bleaching. Gland, Switzerland: IUCN; 2006. Report No.: 2831709504.
  82. 82. Millar CI, Stephenson NL, Stephens SL. Climate change and forests of the future: managing in the face of uncertainty. Ecological applications. 2007;17(8):2145–51. pmid:18213958
  83. 83. Poff NL. Ecological response to and management of increased flooding caused by climate change. Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences. 2002;360(1796):1497–510.
  84. 84. Hernández-Miranda E, Veas R, Labra FA, Salamanca M, Quiñones RA. Response of the epibenthic macrofaunal community to a strong upwelling-driven hypoxic event in a shallow bay of the southern Humboldt Current System. Marine environmental research. 2012;79:16–28. pmid:22626877
  85. 85. Clarke K, Warwick R. Quantifying structural redundancy in ecological communities. Oecologia. 1998;113(2):278–89.
  86. 86. Schaffner LC. Patterns and rates of recovery of macrobenthic communities in a polyhaline temperate estuary following sediment disturbance: effects of disturbance severity and potential importance of non-local processes. Estuaries and Coasts. 2010;33(6):1300–13.
  87. 87. Isaac JL, Vanderwal J, Johnson CN, Williams SE. Resistance and resilience: quantifying relative extinction risk in a diverse assemblage of Australian tropical rainforest vertebrates. Diversity and Distributions. 2009;15(2):280–8.
  88. 88. Huang Y, Martin L, Isbell F, Wilsey B. Is community persistence related to diversity? A test with prairie species in a long-term experiment. Basic and applied ecology. 2013;14(3):199–207.
  89. 89. Kahmen A, Perner J, Buchmann N. Diversity-dependent productivity in semi-natural grasslands following climate perturbations. Functional Ecology. 2005;19(4):594–601.
  90. 90. Frazier AE, Renschler CS, Miles SB. Evaluating post-disaster ecosystem resilience using MODIS GPP data. International Journal of Applied Earth Observation and Geoinformation. 2013;21:43–52.
  91. 91. Sundstrom SM, Allen CR, Barichievy C. Species, functional groups, and thresholds in ecological resilience. Conservation Biology. 2012;26(2):305–14. pmid:22443132
  92. 92. Aung TT, Mochida Y, Than MM. Prediction of recovery pathways of cyclone-disturbed mangroves in the mega delta of Myanmar. Forest ecology and management. 2013;293:103–13.
  93. 93. Brunel T, Piet GJ. Is age structure a relevant criterion for the health of fish stocks? ICES Journal of Marine Science: Journal du Conseil. 2013:fss184.
  94. 94. D'Odorico P, Bhattachan A. Hydrologic variability in dryland regions: impacts on ecosystem dynamics and food security. Phil Trans R Soc B. 2012;367(1606):3145–57. pmid:23045712
  95. 95. Allison G. The influence of species diversity and stress intensity on community resistance and resilience. Ecological Monographs. 2004;74(1):117–34.
  96. 96. Hughes AR, Stachowicz JJ. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(24):8998–9002. pmid:15184681
  97. 97. Brewer JS. Disturbance-mediated competition between perennial plants along a resource supply gradient. Journal of Ecology. 2011;99(5):1219–28.
  98. 98. Marshall KN, Hobbs NT, Cooper DJ. Stream hydrology limits recovery of riparian ecosystems after wolf reintroduction. Proceedings of the Royal Society of London B: Biological Sciences. 2013;280(1756):20122977.
  99. 99. Jaunatre R, Buisson E, Muller I, Morlon H, Mesléard F, Dutoit T. New synthetic indicators to assess community resilience and restoration success. Ecological indicators. 2013;29:468–77.
  100. 100. Paine RT. Food webs: linkage, interaction strength and community infrastructure. Journal of Animal Ecology. 1980;49(3):667–85.
  101. 101. Doerr VA, Barrett T, Doerr ED. Connectivity, dispersal behaviour and conservation under climate change: a response to Hodgson et al. Journal of Applied Ecology. 2011;48(1):143–7.
  102. 102. Bisson PA, Dunham JB, Reeves GH. Freshwater ecosystems and resilience of Pacific salmon: habitat management based on natural variability. 2009.
  103. 103. Schindler DE, Hilborn R, Chasco B, Boatright CP, Quinn TP, Rogers LA, et al. Population diversity and the portfolio effect in an exploited species. Nature. 2010;465(7298):609–12. pmid:20520713
  104. 104. Reusch TB, Ehlers A, Hämmerli A, Worm B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(8):2826–31. pmid:15710890
  105. 105. Bell G, Gonzalez A. Evolutionary rescue can prevent extinction following environmental change. Ecology letters. 2009;12(9):942–8. pmid:19659574
  106. 106. Awiti A. Biological diversity and resilience: lessons from the recovery of cichlid species in Lake Victoria. Ecology and Society. 2011;16(1):1.
  107. 107. Proença V, Pereira HM, Vicente L. Resistance to wildfire and early regeneration in natural broadleaved forest and pine plantation. Acta Oecologica. 2010;36(6):626–33.
  108. 108. Di Carlo G, Kenworthy WJ. Evaluation of aboveground and belowground biomass recovery in physically disturbed seagrass beds. Oecologia. 2008;158(2):285–98. pmid:18830634
  109. 109. Elmhirst T, Connolly SR, Hughes TP. Connectivity, regime shifts and the resilience of coral reefs. Coral Reefs. 2009;28(4):949–57.
  110. 110. Gunderson LH. Ecological resilience—in theory and application. Annual review of ecology and systematics. 2000:425–39.
  111. 111. Grime J. Plant strategies, vegetation processes, and ecosystem properties–John Wiley and Sons Ltd. Chichester, England. 2002.
  112. 112. Ehlers A, Worm B, Reusch TB. Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Marine Ecology Progress Series. 2008;355:1–7.
  113. 113. McClanahan TR, Donner SD, Maynard JA, MacNeil MA, Graham NA, Maina J, et al. Prioritizing key resilience indicators to support coral reef management in a changing climate. PloS one. 2012;7(8):e42884. pmid:22952618
  114. 114. Robinson CT. Long-term changes in community assembly, resistance, and resilience following experimental floods. Ecological Applications. 2012;22(7):1949–61. pmid:23210311
  115. 115. del Castillo RF, Trujillo-Argueta S, Sánchez-Vargas N, Newton AC. Genetic factors associated with population size may increase extinction risks and decrease colonization potential in a keystone tropical pine. Evolutionary applications. 2011;4(4):574–88. pmid:25568006
  116. 116. Mijatović D, Van Oudenhoven F, Eyzaguirre P, Hodgkin T. The role of agricultural biodiversity in strengthening resilience to climate change: towards an analytical framework. International journal of agricultural sustainability. 2013;11(2):95–107.
  117. 117. Stagg CL, Mendelssohn IA. Controls on resilience and stability in a sediment-subsidized salt marsh. Ecological Applications. 2011;21(5):1731–44. pmid:21830714
  118. 118. Norkko J, Norkko A, Thrush SF, Valanko S, Suurkuukka H. Conditional responses to increasing scales of disturbance, and potential implications for threshold dynamics in soft-sediment communities. Marine Ecology Progress Series. 2010;413:253–66.
  119. 119. Middleton BA. The flood pulse concept in wetland restoration. Flood pulsing in wetlands: Restoring the natural hydrological balance. 2002:1–10.
  120. 120. Benedetti-Cecchi L, Bertocci I, Vaselli S, Maggi E. Temporal variance reverses the impact of high mean intensity of stress in climate change experiments. Ecology. 2006;87(10):2489–99. pmid:17089658
  121. 121. Donohue I, Leira M, Hobbs W, León-Vintró L, O'Reilly J, Irvine K. Rapid ecosystem recovery from diffuse pollution after the Great Irish Famine. Ecological Applications. 2010;20(6):1733–43. pmid:20945771
  122. 122. Machtans CS, Villard MA, Hannon SJ. Use of riparian buffer strips as movement corridors by forest birds. Conservation biology. 1996;10(5):1366–79.
  123. 123. Norden N, Chazdon RL, Chao A, Jiang YH, Vílchez-Alvarado B. Resilience of tropical rain forests: tree community reassembly in secondary forests. Ecology Letters. 2009;12(5):385–94. pmid:19379133
  124. 124. Brauns M, Gücker B, Wagner C, Garcia XF, Walz N, Pusch MT. Human lakeshore development alters the structure and trophic basis of littoral food webs. Journal of Applied Ecology. 2011;48(4):916–25.
  125. 125. Angelini C, Silliman BR. Patch size-dependent community recovery after massive disturbance. Ecology. 2012;93(1):101–10. pmid:22486091
  126. 126. Bernhardt JR, Leslie HM. Resilience to climate change in coastal marine ecosystems. Marine Science. 2013;5.
  127. 127. Gerisch M, Dziock F, Schanowski A, Ilg C, Henle K. Community resilience following extreme disturbances: The response of ground beetles to a severe summer flood in a Central European lowland stream. River Research and Applications. 2012;28(1):81–92.
  128. 128. Shuman JK, Shugart HH. Resilience and stability associated with conversion of boreal forest: INTECH Open Access Publisher; 2012.
  129. 129. Connolly S, Lopez-Yglesias M, Anthony K. Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs. 2012;31(4):951–60.
  130. 130. Stachowicz JJ, Graham M, Bracken ME, Szoboszlai AI. Diversity enhances cover and stability of seaweed assemblages: the role of heterogeneity and time. Ecology. 2008;89(11):3008–19.
  131. 131. Viejo RM. Resilience in intertidal rocky shore assemblages across the stress gradient created by emersion times. Marine Ecology Progress Series. 2009;390:55–65.
  132. 132. Banning NC, Murphy DV. Effect of heat-induced disturbance on microbial biomass and activity in forest soil and the relationship between disturbance effects and microbial community structure. Applied Soil Ecology. 2008;40(1):109–19.
  133. 133. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS. Recovery of an isolated coral reef system following severe disturbance. Science. 2013;340(6128):69–71. pmid:23559247
  134. 134. Herrick JE, Schuman GE, Rango A. Monitoring ecological processes for restoration projects. Journal for Nature Conservation. 2006;14(3):161–71.
  135. 135. Adger WN, Hughes TP, Folke C, Carpenter SR, Rockström J. Social-ecological resilience to coastal disasters. Science. 2005;309(5737):1036–9. pmid:16099974
  136. 136. Randall Hughes A, Stachowicz JJ. Seagrass genotypic diversity increases disturbance response via complementarity and dominance. Journal of Ecology. 2011;99(2):445–53.
  137. 137. Crabbe MJC. Topography and spatial arrangement of reef-building corals on the fringing reefs of North Jamaica may influence their response to disturbance from bleaching. Marine Environmental Research. 2010;69(3):158–62. pmid:19819006
  138. 138. Lundquist CJ, Thrush SF, Coco G, Hewitt JE. Interactions between disturbance and dispersal reduce persistence thresholds in a benthic community. Marine Ecology Progress Series. 2010;413:217–28.
  139. 139. Van Ruijven J, Berendse F. Diversity enhances community recovery, but not resistance, after drought. Journal of Ecology. 2010;98(1):81–6.
  140. 140. Bellwood DR, Hughes TP, Folke C, Nyström M. Confronting the coral reef crisis. Nature. 2004;429(6994):827–33. pmid:15215854
  141. 141. Clark JM, Kershner MW. Short-and long-term impacts of a major flood event on crayfish (Orconectes obscurus) in a forested stream. Fundamental and Applied Limnology/Archiv für Hydrobiologie. 2011;179(3):225–33.
  142. 142. Carter DL, Blair JM. High richness and dense seeding enhance grassland restoration establishment but have little effect on drought response. Ecological Applications. 2012;22(4):1308–19. pmid:22827137
  143. 143. Naiman RJ, Bilby RE, Bisson PA. Riparian ecology and management in the Pacific coastal rain forest. BioScience. 2000;50(11):996–1011.
  144. 144. Beechie T, Bolton S. An approach to restoring salmonid habitat-forming processes in Pacific Northwest watersheds. Fisheries. 1999;24(4):6–15.
  145. 145. Naiman RJ, Decamps H, Pollock M. The role of riparian corridors in maintaining regional biodiversity. Ecological applications. 1993;3(2):209–12. pmid:27759328
  146. 146. Lirman D, Manzello D. Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. Journal of Experimental Marine Biology and Ecology. 2009;369(1):72–7.
  147. 147. Naeem S, Li S. Biodiversity enhances ecosystem reliability. Nature. 1997;390(6659):507–9.
  148. 148. Noss RF. Beyond Kyoto: forest management in a time of rapid climate change. Conservation Biology. 2001;15(3):578–90.
  149. 149. Jacquet K, Prodon R. Measuring the postfire resilience of a bird–vegetation system: a 28-year study in a Mediterranean oak woodland. Oecologia. 2009;161(4):801–11. pmid:19727831
  150. 150. Eldridge DJ, Lunt ID. Resilience of soil seed banks to site degradation in intermittently flooded riverine woodlands. Journal of Vegetation Science. 2010;21(1):157–66.
  151. 151. Milner AM, Robertson AL, McDermott MJ, Klaar MJ, Brown LE. Major flood disturbance alters river ecosystem evolution. Nature Climate Change. 2013;3(2):137–41.
  152. 152. Pimm SL. The complexity and stability of ecosystems. Nature. 1984;307(5949):321–6.
  153. 153. Emmerson M, Yearsley JM. Weak interactions, omnivory and emergent food-web properties. Proceedings of the Royal Society of London B: Biological Sciences. 2004;271(1537):397–405.
  154. 154. Duffy JE. Why biodiversity is important to the functioning of real-world ecosystems. Frontiers in Ecology and the Environment. 2009;7(8):437–44.
  155. 155. Van den Brink FW, Van der Velde G, Wijnhoven S. Diversity, occurrence and feeding traits of caddisfly larvae as indicators for ecological integrity of river-floodplain habitats along a connectivity gradient. Ecological indicators. 2013;25:92–8.
  156. 156. Chapin FS, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, et al. Biotic control over the functioning of ecosystems. Science. 1997;277(5325):500–4.
  157. 157. Mumby PJ, Hastings A. The impact of ecosystem connectivity on coral reef resilience. Journal of Applied Ecology. 2008;45(3):854–62.
  158. 158. Gergel SE, Dixon MD, Turner MG. CONSEQUENCES OF HUMAN-ALTERED FLOODS: LEVEES, FLOODS, AND FLOODPLAIN FORESTS ALONG THE WISCONSIN RIVER. Ecological applications. 2002;12(6):1755–70.
  159. 159. Eklöf JS, McMahon K, Lavery PS. Effects of multiple disturbances in seagrass meadows: shading decreases resilience to grazing. Marine and Freshwater Research. 2010;60(12):1317–27.
  160. 160. López DR, Brizuela MA, Willems P, Aguiar MR, Siffredi G, Bran D. Linking ecosystem resistance, resilience, and stability in steppes of North Patagonia. Ecological indicators. 2013;24:1–11.
  161. 161. Robertson AL. Lotic meiofaunal community dynamics: colonisation, resilience and persistence in a spatially and temporally heterogeneous environment. Freshwater Biology. 2000;44(1):135–47.
  162. 162. Sahib N, Rhazi L, Grillas P. Post-disturbance dynamics of plant communities in a Mediterranean temporary pool (Western Morocco): Effects of disturbance size. Botany. 2011;89(2):105–18.
  163. 163. Arthington ÁH, Naiman RJ, McClain ME, Nilsson C. Preserving the biodiversity and ecological services of rivers: new challenges and research opportunities. Freshwater Biology. 2010;55(1):1–16.
  164. 164. McNaughton SJ. Diversity and stability of ecological communities: a comment on the role of empiricism in ecology. American Naturalist. 1977:515–25.
  165. 165. Cowling R, Pressey R. Rapid plant diversification: planning for an evolutionary future. Proceedings of the national academy of sciences. 2001;98(10):5452–7.
  166. 166. Leigh C. Dry-season changes in macroinvertebrate assemblages of highly seasonal rivers: responses to low flow, no flow and antecedent hydrology. Hydrobiologia. 2013;703(1):95–112.
  167. 167. Simenstad C, Reed D, Ford M. When is restoration not?: Incorporating landscape-scale processes to restore self-sustaining ecosystems in coastal wetland restoration. Ecological Engineering. 2006;26(1):27–39.
  168. 168. Gough CM, Hardiman BS, Nave LE, Bohrer G, Maurer KD, Vogel CS, et al. Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest. Ecological Applications. 2013;23(5):1202–15. pmid:23967586
  169. 169. Lin T-C, Hamburg SP, Lin K-C, Wang L-J, Chang C-T, Hsia Y-J, et al. Typhoon disturbance and forest dynamics: lessons from a northwest Pacific subtropical forest. Ecosystems. 2011;14(1):127–43.
  170. 170. Dunne JA, Williams RJ, Martinez ND. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology letters. 2002;5(4):558–67.
  171. 171. Skidmore P, Beechie T, Pess G, Castro J, Cluer B, Thorne C, et al. Developing, designing, and implementing restoration projects. Stream and Watershed Restoration: A Guide to Restoring Riverine Processes and Habitats. 2013:215–53.
  172. 172. van de Koppel J, Rietkerk M. Spatial interactions and resilience in arid ecosystems. The American Naturalist. 2004;163(1):113–21. pmid:14767841
  173. 173. Hilty JA, Merenlender AM. Use of riparian corridors and vineyards by mammalian predators in northern California. Conservation Biology. 2004;18(1):126–35.
  174. 174. Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, et al. Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS One. 2009;4(4):e5239. pmid:19384423
  175. 175. Bêche LA, Connors PG, Resh VH, Merenlender AM. Resilience of fishes and invertebrates to prolonged drought in two California streams. Ecography. 2009;32(5):778–88.
  176. 176. Mariotte P, Vandenberghe C, Kardol P, Hagedorn F, Buttler A. Subordinate plant species enhance community resistance against drought in semi-natural grasslands. Journal of Ecology. 2013;101(3):763–73.
  177. 177. Williams SL. Reduced genetic diversity in eelgrass transplantations affects both population growth and individual fitness. Ecological Applications. 2001;11(5):1472–88.
  178. 178. Virah-Sawmy M, Gillson L, Willis KJ. How does spatial heterogeneity influence resilience to climatic changes? Ecological dynamics in southeast Madagascar. Ecological Monographs. 2009;79(4):557–74.
  179. 179. Griffiths B, Hallett P, Kuan H, Gregory A, Watts C, Whitmore A. Functional resilience of soil microbial communities depends on both soil structure and microbial community composition. Biology and Fertility of Soils. 2008;44(5):745–54.
  180. 180. de Vries FT, Liiri ME, Bjørnlund L, Setälä HM, Christensen S, Bardgett RD. Legacy effects of drought on plant growth and the soil food web. Oecologia. 2012;170(3):821–33. pmid:22555357
  181. 181. Zhang B, Wang H, Yao S, Bi L. Litter quantity confers soil functional resilience through mediating soil biophysical habitat and microbial community structure on an eroded bare land restored with mono Pinus massoniana. Soil Biology and Biochemistry. 2013;57:556–67.
  182. 182. Yount JD, Niemi GJ. Recovery of lotic communities and ecosystems from disturbance—a narrative review of case studies. Environmental Management. 1990;14(5):547–69.
  183. 183. White JM, Stromberg JC. Resilience, restoration, and riparian ecosystems: case study of a dryland, urban river. Restoration Ecology. 2011;19(1):101–11.
  184. 184. Karr JR, Fausch KD, Angermeier PL, Yant PR, Schlosser IJ. Assessing biological integrity in running waters. A method and its rationale Illinois Natural History Survey, Champaign, Special Publication. 1986;5.
  185. 185. South Florida Environmental Report Highlights South Florida Water Management District [Internet] http://my.sfwmd.gov/portal/page/portal/xweb%20about%20us/agency%20reports.
  186. 186. McElhany P, Ruckelshaus M, Ford M, Wainwright T, Bjorkstedt E. Viable salmonid populations and the recovery of evolutionarily significant units. US Dept. Commer. NOAA Tech Memo NMFS-NWFSC. 2000;42:156.
  187. 187. Selig ER, Bruno JF. A global analysis of the effectiveness of marine protected areas in preventing coral loss. PLoS One. 2010;5(2):e9278. pmid:20174644
  188. 188. Walton A, White AT, Tighe S, Aliño PM, Laroya L, Dermawan A, et al. Establishing a functional region-wide Coral Triangle marine protected area system. Coastal Management. 2014;42(2):107–27.
  189. 189. Conservation Methods: NOAA Coral Reef Conservation Program [Internet]; [2016 May 3]. http://coralreef.noaa.gov/conservation/methods/.
  190. 190. Force IOPT. Final recommendations of the interagency ocean policy task force. Washington, DC: The White House Council on Environmental Quality. 2010.
  191. 191. WDFW Climate News Digest http://wdfw.wa.gov/conservation/climate_change/digest/climate_change_digest_2013_04.pdf.