Impact of Ecological Restoration on Ecosystem Services

Impact of Ecological Restoration on Ecosystem Services Holly P Jones, University of California, Santa Cruz, CA, USA r 2013 Elsevier Inc. All rights reserved.

Glossary Active restoration Actively assisting a system in recovery beyond removing the disturbance. Ecosystem engineers Species that modify, maintain, or create habitats and modify resource supplies through either their physical structure or by transforming living materials from one state to another. Ecosystem services Those products or services that nature provides society. Keystone species Species that have a disproportionate effect on ecosystems relative to their biomass.

Ecological Restoration As resource use and human populations grow (Haberl et al., 2004; United Nations, 2004), restoration of degraded ecosystems is becoming one of the most important tools in conservation managers’ toolboxes (Dobson et al., 1997; Kareiva et al., 2007). Restoration is critical not only to maintain habitat for biodiversity, but also to provide the ecosystem services necessary for human survival (Dobson et al., 1997; Hobbs and Harris, 2001; Foley et al., 2005; MEA (Millennium Ecosystem Assessment), 2005; Kareiva et al., 2007; Benayas et al., 2009). However, restoration can be costly, complex, and labor-intensive and is not always successful, which has traditionally led to reluctance in pursuing large-scale restoration projects (Hobbs and Harris, 2001; Kumar, 2004; van Andel and Aronson, 2006; Jentsch, 2007). If restoration is to succeed in the context of limited funding and capacity, calculating the value of restoration projects is absolutely critical. As our ability to value ecosystem services continues to develop, the return on investment of restoration projects increasingly looks favorable, even for large-scale restoration projects (TEEB, 2010). This article will discuss the concepts of ecological restoration, ecosystem services, and how they are being merged to show society what it stands to gain from restoring earth’s damaged ecosystems.

What is Ecological Restoration? Ecological restoration has been in practice for centuries. For example, Native Americans in the Washington Cascades lit periodic forest fires to sustain natural ecosystem services, such as food crops and game animal forage (Everett et al., 2000). Despite centuries of restoration projects, restoration ecology was not formally recognized as its own scientific discipline until the 1990s (Allen et al., 1997). Until then, grass-roots restoration projects were common throughout the world in the form of invasive species removal (Howald et al., 2007), native species introductions (Towns and Ferreira, 2001), and

Encyclopedia of Biodiversity, Volume 4

Nonuse ecosystem services Benefits which are derived from ecosystems without using them (e.g., existence values – the benefit we derive from knowing something exists). Novel ecosystems Systems that have conditions and combinations of organisms never seen in the historical past. Passive recovery Allowing a system to recover on its own without intervention beyond removing the disturbance. Restoration The process of assisting in the recovery of damaged, degraded, or destroyed ecosystems.

native plant revegetation (D’Antonio et al., 1992). However, most of these projects did not have a common theoretical framework and consisted of a hodgepodge of strategies, goals, successes, and failures (Hobbs and Norton, 1996). Starting in the 1990s, this incoherence began to change (Hobbs and Norton, 1996; Allen et al., 1997). The National Science Foundation began to expressly request proposals for restoration ecology, and scientists began devising a theoretical framework from which to practice restoration. Current restoration ecology is not like that of the past, because it is now based around sound ecological principals and it uses theoretical frameworks to design experiments. That said, it is still developing and has much progress ahead of it. In fact, the first textbook for use in classroom teachings was only recently published (van Andel and Aronson, 2006). The Society for Ecological Restoration defines ecological restoration as the process of assisting the recovery of damaged, degraded, or destroyed ecosystems (SER, 2002). This can include removing the original cause of damage and allowing the system to recover on its own (passive recovery), or actively assisting the system in recovery (active restoration). It is important to distinguish passive recovery and active restoration because each has much different costs, capacity needs, and methodology. If systems can recover passively after the agent of damage has been removed, less money, staff, and commitment will be necessary to repair that system. However, ecosystems that need active restoration to recover will require much more time, money, and effort. Restoration ecologists have begun to design a framework from which to plan restoration projects to remedy the ubiquitous restoration projects built with little ecological knowledge and oftentimes unclear or unattainable restoration goals. It is now widely accepted that the first step of a restoration project is to define the goals of the project clearly. Project goals of ‘‘restoring native vegetation’’ or ‘‘recovering a preperturbation state’’ are unacceptable; rather, specific goals of restoring species from X to Y abundance or recovering 85% of natural floodplains on a particular watershed are strived for. The second requirement for a restoration goal is that it should

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be realistic. With the belief that ecosystems are dynamic entities (Pickett and Parker, 1994), restoration ecologists realize that restoring something to a state in the past may not be possible, and rather, the goal should focus on societal expectations for the future (van Andel and Aronson, 2006). The third requirement of a restoration goal is that progress toward the goal should be measured explicitly. One thing that distinguishes restoration ecology from most other hard sciences is its explicit inclusion of societal values in its goals. People set restoration goals, meaning goals are often selected according to subjective views of what society needs or wants from a particular ecosystem. The use of the terms like ‘‘ecosystem health’’ and ‘‘ecosystem integrity,’’ as definitions for restored systems have been particularly controversial. Ecosystem health is defined as ‘‘the state or condition of an ecosystem in which its dynamic attributes are expressed within the normal ranges of activity relative to its ecological state of development’’ (van Andel and Aronson, 2006), while ecosystem integrity is ‘‘the state or condition of an ecosystem that displays the biodiversity characteristic of the reference, such as species composition and community structure, and is fully capable of sustaining normal ecosystem functioning’’ (SER, 2002). Both definitions take the concepts of ecosystem perturbation, resistance, and resilience and add an aspect of societal expectations (van Andel and Aronson, 2006). Integrating society into ecological terms outrages some ecologists (Lancaster, 2000; Davis and Slobodkin, 2004), but restoration ecology, unlike conventional sciences, aims to explicitly incorporate societal expectations into restoration programs. One promising way of incorporating society into restoration goals is using ecosystem services to calculate the value of restoring nature to meet human needs.

Restoration Targets One significant issue for restoration ecology is the definition of a preperturbation state, which, unless resolved, can leave enduring confusion and ambiguous restoration targets. Some restoration ecologists have argued against the use of historical reference data to attain restoration goals for several reasons. First, any attempt to restore systems perturbed by human activity must address the question of how far back in history to go (Diamond, 1987; Hobbs, 2005). In addition, historical and paleontological records are often lacking or incomplete. Finally, using historical reference sites may be very difficult or just impossible because under climate change, shifts of carbon cycles, climate regimes, sea level, and climatic events will change the biophysical make-up of ecosystems to make historical systems difficult or impossible to recreate (Hobbs et al., 2006). Many restoration projects have moved away from the idea of restoring back to ‘‘natural’’ or prehuman ecosystems, and instead, use existing reference systems that have not been exposed to the perturbation (contemporaneous reference sites) as restoration targets (Harris and Diggelen, 2006). The advantages of modern reference systems are that they reflect contemporary climate regimes, have shown resilience to human activity, and have properties that can be explicitly measured to evaluate restoration progress. Another possible

target for restoration is the functional target (Harris and Diggelen, 2006). This is the idea of using ecosystem function parameters such as primary productivity, energy flow, and perturbation regime as restoration targets. However, these properties cannot be easily manipulated and thus make difficult goals to achieve without considering what community type would approach these targets. Finally, some projects aim to restore a suite of ecosystem services to society (Harris and Diggelen, 2006). Using ecosystem service targets can help mangers gain society’s support for restoration by detailing the benefits of restoration in a currency that everyone understands.

Restoring Entire Ecosystems, a Few Ecosystem Drivers, or Ecosystem Services There has been significant debate over whether to restore entire ecosystems or just a few ecosystem drivers (Goldstein, 1999; Risser, 1999; Walker, 1999), and it is complicated by divergent views about the nature of communities and ecosystems. Ecosystems can be viewed as stocks and flows of their biotic and abiotic components, which is an entire ecosystem view (Odum, 1969). An alternative view is that ecosystems are composed of communities of species pitted against one another in outright Darwinian evolutionary struggles, and only a few of these influence the entire community, which is an ecosystem driver view (Oksanen, 1988). Both perspectives have advantages and disadvantages for restoration ecology. A restoration project that focuses on ecosystem drivers emphasizes key components of ecosystems, may enhance biodiversity, and can require less time and cost to carry out than whole-ecosystem restorations. However, this focus on single species or small groups of species fails to recognize the importance of processes at the landscape scale, assumes untested links between components of communities, may inadvertently damage species not targeted in restoration, and may divert attention from other important species (Ehrenfeld, 2000). The ecosystem view, however, recognizes the importance of landscape-scale processes to species persistence, incorporates the view that systems are dynamic, and can help to encourage participation from a variety of agencies and stakeholders. However, attempting to restore entire ecosystems is complicated because ecosystem functions are difficult to define or measure. Even with adequate definitions, functions sometimes do not correlate with each other and often operate on different temporal and spatial scales. This makes realistic restoration goals difficult to set. The third concept is the ecosystem services view (Ehrenfeld, 2000). Projects with goals of restoring ecosystem services have clearly identified goals and tend to generate public support and funding. However, such projects may have difficult-to-measure services, are contingent upon willingness-to-pay, must overcome trade-offs between equally desirable ecosystem services, and could be compromised if changes in society, technology, or the economy devalue the services that such projects are targeting. Ecosystem services are difficult to distinguish from the ecosystem view because restoring ecosystem services requires restoring the same ecosystem functions that are the targets of whole-ecosystem restoration projects. As such, the ecosystem service viewpoint can be seen as a strategy

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to justify restoration rather than a completely different viewpoint. Each of these views for setting restoration goals has advantages and disadvantages. No one paradigm is correct for restoration – instead, each one should be considered in turn before deciding which paradigm is appropriate for the focal restoration project. In many cases, more than one paradigm will apply. For example, restoring an entire watershed must focus on landscape-scale processes such as hydrologic flows, river diversions, and runoff control. Ecosystem driver restoration goals are unrealistic in this case because its scope is well beyond restoring one or a few species. However, wholeecosystem goals and ecosystem service goals are both appropriate. Whole-ecosystem frameworks can be used to help define the restoration targets, while ecosystem services can be used to help generate public support for the project. Attempting to create universally applicable laws may not be necessary for restoration as it is such a broad, diverse, and complex discipline (Ehrenfeld, 2000). Instead, using common sense principles to decide which framework works for each unique situation will ensure each restoration project has a better chance of reaching the goals that are appropriate in each context. Below are examples of projects that use each framework as the basis for setting restoration goals.

Restoration of Ecosystem Drivers Some ecosystems seem to be largely driven by one or a few species, in terms of ecosystem structure or function. Keystone species are one example of ecosystem-driving species and they are so named because they are akin to a keystone that supports an entire arch – without the keystone, the entire arch would collapse (Paine, 1995). Keystone species have a disproportionate effect on ecosystems relative to their biomass and when they are affected or removed by a perturbation, the effects on ecosystems can be tremendous (Paine, 1966). Sea otters are a classic example of a keystone species in ocean kelp forests. Otters prefer to consume herbivorous invertebrates such as sea urchins, which are particularly voracious consumers of kelp. When otters are removed from the system (which occurred extensively along the west coast of North America in the 1800s due to otter hunting for pelts), invertebrate populations explode and quickly consume and destroy the kelp forests, which results in the collapse of an entire system – without the kelp, fish and invertebrate species lose their habitat, and abiotic conditions (light, nutrient availability) fundamentally change (Estes and Duggins, 1995). Kelp forests that have been destroyed by uncontrolled herbivorous invertebrates have been termed urchin barrens because all that is left are large populations of urchins. In this way, the loss or reduction of a single species can result in devastating losses to ecosystem services including opportunities for recreation, commercial fishing nursery grounds, and carbon sequestration. Other species thought to be the key drivers of ecosystem structure or function are termed ecosystem engineers. These species modify, maintain, or create habitats and modify resource supplies through either their physical structure (e.g., trees in forests), or by their transforming living materials from one state to another (e.g., beavers building dams; Jones et al., 1994). Coral reefs are classic examples of ecosystem engineers.

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Their structure changes the coastal environment and modifies the abundance and distribution of resources (e.g., light, nutrient availability), and protects entire reef systems and coastal ecosystems from water force and wave action (Anderson, 1992; Moberg and Ro¨nnba¨ck, 2003). This makes perturbations to corals especially dramatic because they alter entire ecosystems as opposed to just one species. Loss of corals reduces the ecosystem services that corals provide – commercially important fish and invertebrate species lose their habitat, coastal communities are less protected from storm surges and wave action, and recreational and tourist opportunities are diminished. Restoring systems that have lost their keystone species or ecosystem engineers usually consists of restoring the species to its historical location. For example, over the past century, riparian ecosystems in much of the western US have been lost from large-scale recruitment failures of key riparian tree species like native cottonwoods and aspens. Mounting evidence has suggested that these failures were due to the system losing its top predators – wolves – from human hunting pressures in the 1920s (Vander Zanden et al., 2006). The loss of wolves led elk to change their foraging behavior and forage for cottonwoods and aspens without fear of predation from wolves (Ripple et al., 2001; Beschta, 2003). Wolves were reintroduced in the mid-1990s and their regulation of elk populations and foraging behavior has allowed riparian vegetation to recover. This recovery is expected to improve bird nesting habitat, stabilize stream banks, strengthen ecosystem linkages, and moderate water temperatures (Osborne and Kovacic, 1993; Berger et al., 2001). In this case, reestablishment of one keystone species has carried over to the entire ecosystem. It illustrates the relative simplicity of restoring systems that have lost only one of their key species.

Whole-ecosystem Restoration Restoring entire ecosystems is an ambitious undertaking. Whole-ecosystem restoration involves repairing or restoring most if not all of the functions of an ecosystem following a perturbation. It most often refers to restoration projects at the landscape scale and is arguably one of the most efficient ways to bolster ecosystem services because restoring such large-scale processes results in provisioning of a wealth of ecosystem services at vast scales. For example, efforts to restore the Mississippi–Ohio–Missouri river basin following eutrophication from farm runoff is projected to reduce hypoxia in the Gulf of Mexico, improve water quality for commercially important fish and invertebrate species, provide large swaths of riparian floodplains to help regulate floodwaters for people and croplands, improve water quality and quantity for local residents, and provide habitat for local wildlife (Mitsch and Day, 2006). This single restoration action, carried out by various organizations and covering multiple states, and millions of hectares, has the potential for a much larger ecosystem service benefit than smaller-scale restorations aimed at one or a few species or habitats. It is also significantly more complex because it covers more habitats, ecosystem processes, species, and jurisdictions than smaller-scale restorations. As such, it is a good illustration of both the immense benefits and challenges of attempting to restore entire ecosystems.

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Ecosystem Service Restoration Since the seminal works defining ecosystem services – also known as natural capital (Daily, 1997) – and valuing them (Costanza et al., 1997), restoration ecology has been increasingly focused on restoring not just species or ecosystems, but also ecosystem service values. Ecosystem services are increasingly called for as a means to justify restoration, set goals that are more realistic than historical targets given continuing climate and global change, and to illustrate the connection between people and nature (Cairns, 2000; Hobbs and Cramer, 2008; Chazdon et al., 2009; Jackson and Hobbs, 2009). Ecosystem services are those products or services that nature provides society. There are many different ways to categorize ecosystem services, but most are blocked into four main types (MEA, 2005): provisioning – those that provide a product such as croplands provide food; regulating – those that provide regulation of function such as coastal wetlands provide wave attenuation for coastal populations faced with tropical storms (Alongi, 2008; Das and Vincent, 2009; Shepard et al., 2011); support – those that support other ecosystem services such as primary production; and cultural – those that provide cultural, aesthetic, or spiritual benefits such as national parks provide recreational opportunities. Ecosystem services are covered extensively elsewhere in this volume, so they are discussed only in reference to restoration in this article. Ecosystems naturally provide some of these benefits whether they are degraded or intact, but intact systems have higher potential for ecosystem services than do degraded ones (Chazdon, 2008; Benayas et al., 2009). This is where ecological restoration and ecosystem services combine – restoration can help ecosystems regain their function and thereby increase the potential for ecosystems to provide services to humankind. Restoring ecosystem services, then, requires restoring the underlying ecosystem functions that relate to the desired services. Each service relies on an underlying ecosystem process for its production. For example, Table 1 lists some common ecosystem services, ecosystems, and what ecosystem process is necessary for each service. As the table illustrates, restoring ecosystem services is no different than restoring key ecosystem functions. Instead, using ecosystem services as a target for restoration is a way to communicate how society will benefit from restoring key ecosystem functions, generate public support, and generate funding mechanisms for restoration projects.

It is still difficult to glean examples of restoration projects whose specific goals were to recover ecosystem services. This stems from issues inherent in defining the functions needed to restore the service, an incomplete understanding of ecosystem dynamics, and from the disconnect between ecological and economic understanding of ecosystem service restoration (Kremen, 2005; Palmer and Filoso, 2009; Wegner and Pascual, 2011). Instead, it is more common to use ecosystem service targets as a call to restore. For example, a model was recently developed for The Drakensberg Mountains of South Africa to calculate the economic benefits of restoring degraded grasslands and riparian zones as ways to increase the low base water flows during the winter months (Mander et al., 2008). The restoration would cost around $5.1 million over 7 years, while the ecosystem service benefits of additional water, sediment reduction, and carbon sequestration are valued at $8.4 million per year (Blignaut et al., 2010). The study and many other similar studies (Loomis et al., 2000; Tong et al., 2007; Yu et al., 2009) provide the motivation behind large-scale restoration projects that attempt to align nature with societal goals. A second way that ecosystem services are incorporated into restoration is through hindsight. Ecosystems throughout the world have been restored, but the concept of ecosystem services is so new that it is more common to calculate the ecosystem service benefits of past restoration projects, or to frame past projects in terms of ecosystem services now that we know how effective ecosystem services can be in gathering public support for restoration (e.g., Aronson et al., 2007). For example, the island-scale ecological restoration on Tiritiri Matangi Island, New Zealand, was conceived as a way to restore native flora and fauna, but the ecosystem service benefits of the restoration project are now being touted as some of the greatest benefits of restoration (Craig and Vesely, 2007). As the practice of restoration catches up with the theory of ecosystem services, we will begin to see many restoration projects with specific goals of restoring ecosystem services.

Other Key Considerations for Ecological Restoration Novel Ecosystems The idea that there are novel or synthetic ecosystems – those that have conditions and combinations of organisms never before seen – goes back as far as Odum (1962). Recent work

Table 1 Ten of the most critical ecosystem services for human well-being and the associated ecosystem functions that are critical in providing those services. While ecological restoration can be framed in terms of the ecosystem services restoration provides, it is the underlying ecosystem functions which must be restored to provide those services Ecosystem service

Corresponding ecosystem processes

Air purification Carbon sequestration Climate regulation

Plant respiration, photosynthesis, toxin filtration, nutrient filtration, nutrient cycling Carbon storage, carbon cycling, photosynthesis Carbon storage, carbon cycling, photosynthesis, light absorption, light reflection, evaporation, transpiration Wave attenuation, water absorption, water retention, water storage, land stabilization Pollinator population dynamics Nutrient cycling, nutrient mineralization, water absorption, water retention, nutrient fixing Floodwater absorption, floodwater retention, wave attenuation, water storage Water absorption, water retention, water storage Forest net primary production, photosynthesis Nutrient filtration, toxin filtration, nutrient retention/cycling, water storage

Coastal defense from storms, sea-level rise Crop pollination Fertile soils Flood protection Freshwater provisioning Timber Water purification

Impact of Ecological Restoration on Ecosystem Services

has termed such systems novel ecosystems (also known as ‘‘emerging’’ or ‘‘no-analog’’ systems) and has defined them as those ‘‘containing new combinations of species that arise through human action, environmental change, and the impacts of the deliberate and inadvertent introduction of species from other parts of the world’’ (Hobbs et al., 2009; Marris, 2011). Novel ecosystems are an ambiguous concept because depending on the timeframe of interest, anything could be considered novel. However, the main proponents of using novel ecosystems to help guide restoration efforts suggest that the accelerated pace and breakdown of biogeographic barriers sets current novel ecosystems apart from the past in terms of the increased rate of novel environment appearance, novel species combinations, and altered ecosystem functioning (Hobbs et al., 2009). The utility of terming systems novel seems to move restoration targets away from historical states and instead argues for ecosystem service and ecosystem function restoration goals (Jackson and Hobbs, 2009). This is laudable but much of the debate on using historical reference sites has already been settled and so the introduction of this new terminology is still somewhat puzzling. Novel ecosystems have arbitrary definitions and could therefore represent a range of scenarios from a severely perturbed system to one that has been completely replaced by new species. Another component of the novel system framework is the hybrid ecosystem, which also has an arbitrary definition – somewhere between a novel and an historical system – and cannot be clearly distinguished from just perturbed or novel ecosystems. Indeed, a large perturbation such as logging can result in a complete replacement of the previous vegetation with new, early-successional and possibly invasive grasses. Is this then a novel ecosystem because it is different from the historical past and likely made up of new species combinations? Or is it merely a perturbed system in the beginning stages of recovery? Their arbitrary definitions make novel systems impossible to distinguish from just severely perturbed systems and therefore cause difficulty in identifying the extent of their existence, illustrating their impact, and using them as potential restoration targets. Despite these difficulties, the existence of novel ecosystems is certainly another good argument against using historical references in restoration, but focusing our energy on ambiguously defined and difficult-to-identify ecosystems could also take away from sorely needed advancements in using ecosystem services to calculate return on restoration investments.

Restoration and Global Change It is important to recognize that ecosystem repair from various perturbations is happening against a backdrop of global change that has accelerated at unprecedented rates since the industrial revolution (Baines and Folland, 2007; IPCC, 2007; Maslanik et al., 2007; Belkin, 2009; Gregory et al., 2009). From sea-level rise to heightened hurricane activity, longer and more frequent droughts and floods, and acidification of the world’s oceans, ecosystems are undergoing rapid change (Allison et al., 2009; Fu¨ssel, 2009). This presents an interesting conundrum: How do we choose restoration targets when much of the world’s ecosystem processes are in a state of flux and are likely to continue changing for the foreseeable future? This dynamic and unpredictable climate argues against the use of historical

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baselines for restoration because they will be increasingly impossible to recreate amidst changing biophysical conditions (Harris et al., 2006). Indeed, many have suggested that restoration of processes, rather than historical conditions, will give restoration the best chances of success in a changing world (Harris et al., 2006). In a changing world, our restoration goals are likely to include ecosystems that were never before seen in historical times because we are predicted to experience climate shifts never before realized in such a short time span. The interaction between ecological restoration and global change is an understudied area that will be of rapidly growing interest as we watch systems change before our eyes. Climate change also presents an interesting challenge to legislation that protects critical habitat for species of concern like the Endangered Species Act. Changing ecosystem processes may mean that critical habitats will shift according to species’ biophysical envelopes, and so, protected habitats will no longer be suitable for the species the protection was created for (Harris et al., 2006). Restoration may provide a critical answer to protecting these species – it may be necessary to restore habitats and create shelter for species that will need to migrate given climate change (Harris et al., 2006).

Ecological Restoration and Ecosystem Services Ecosystem Restoration Potential Human population now exceeds seven billion people and this number is projected to grow to eight billion by 2050 (United Nations, 2004). As our population grows, so too do our technological demands, thirst for resources, and exploitation of nature to meet our expanding needs. We have fundamentally altered most ecosystem processes, leaving few areas on Earth untouched by people in some way (Kareiva and Marvier, 2011). Humans have been domesticating nature to meet our needs for centuries (Kareiva et al., 2007), but the rate of ecosystem alteration has spiked since the industrial revolution. As we continue to use nature’s capital to meet our needs, we also threaten to destroy the very resources that we depend on for survival. We have transformed around half of Earth’s surface area to grazing or croplands (MEA, 2005). More than 50% of the world’s forests have been lost through this extreme transformation (MEA, 2005). Although providing food for the masses is a necessary service that ecosystems provide, it is often done at the expense of other ecosystem services such as water quality and quantity regulation, climate regulation, and carbon sequestration. Our insatiable thirst for resources and to control nature has driven the largest mammals on each continent to extinction or severe depletion, fundamentally altering food webs across the globe (Woodroffe, 2000; Lyons et al., 2004). No marine ecosystem on earth is untouched by people and almost half of the world’s oceans face multiple threats (Halpern et al., 2008). As such, there is substantial concern that we are leaving a legacy of extinction, biodiversity loss, and unsustainable exploitation of nature to future generations. Humans are arguably better off now than in previous generations. We are able to feed the masses, control predators, alter natural disturbance regimes, and build infrastructure to help

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protect us from storms. So what has our domination over nature done to the world’s natural capital? The answer is complex because there are trade-offs between different ecosystem services (Kareiva et al., 2007). For example, food provisioning is a service that nature provides but as we replace ecosystems with cropland, other ecosystem services are diminished. Maximizing crop production requires the input of artificial fertilizer, which has caused massive nutrient leaching into waterways and has led to eutrophication of rivers, lakes, estuaries, and oceans. This has led to toxic algal blooms and has created dead zones around the world (Galloway et al., 2003). Similarly, we rely on timber for our furniture, shelter, paper, and other household products. But logging and deforestation has caused soil erosion, which reduces forests’ capacity to absorb floodwaters, reduces water quality, and can alter climate regulation (Daily, 1997; Sweeney et al., 2004; Dobson et al., 2006). We use fossil fuels to travel, heat our homes, produce food, and access water and electricity, but the by-products of this energy demand are increased greenhouse gases and shifting climate regimes that ultimately threaten our very existence (IPCC, 2007). Our marine fisheries and coastal development have depleted 91% of ecologically and economically important coastal marine species to less than 50% of their historical abundances (Worm et al., 2006) and destroyed more than 50% of the world’s mangroves (World Resources Institute, 1996). This severe biodiversity depletion has led to a 33% reduction of fish stocks, a 69% reduction in nursery habitat for marine organisms, and a 63% reduction in water filtration ecosystem services (Worm et al., 2006). So while we have done generally well at taming nature to meet our needs, it has come at a price to ecosystems and the other important services they provide. This price threatens to impact our livelihoods, standard of living, ability to withstand environmental perturbations, and at the most basic level, our persistence. All of these threats may not be realized in our lifetime, but they are very real consequences that will be passed on to future generations. At the same time, there is cause for some optimism. Ecological restoration of ecosystem services offers great promise for restoring the balance between society and nature and to pass on a more hopeful legacy to future generations. As E.O. Wilson so eloquently put it, ‘‘Here is the means to end the great extinction spasm. The next century will, I believe, be the era of restoration in ecology.’’ Combining ecological restoration with ecosystem services can be challenging because they are both such nascent disciplines, there are many trade-offs to study and account for, and the two disciplines (restoration and economics) have so often been at odds with each other in the past. However, the imperative is clear: No place on Earth is untouched by people and so restoring ecosystem services to ensure our future survival will be a key focus of ecological restoration moving forward (Kareiva and Marvier, 2011). Restoring ecosystem services will be one of the most efficient ways to repair ecosystems and ensure human prosperity together in one action.

Bolstering Ecosystem Services as a By-Product of Restoration Many restoration projects that address ecosystem services view them as a co-benefit of restoration rather than a goal of restoration. This is because restoration was historically justified

as a moral imperative (Leopold, 1949). With the realization that moral arguments are not as effective as economic ones, restoration ecologists have increasingly looked at past restoration projects to show how they have benefited society. One of the most comprehensive studies to date illustrating the effects of ecosystem restoration on ecosystem services was a metaanalysis that compared ecosystem services for degraded, restored, and unperturbed reference ecosystems (Benayas et al., 2009). The study showed that restoration increased ecosystem services by 125% relative to degraded systems, giving much hope for restoration to play a key role in repairing nature’s capital. However, ecosystem services were still lower in restored systems versus unperturbed systems, indicating conservation of unperturbed systems will continue to be an important strategy for maintaining ecosystem services. Many other studies illustrate what society stands to gain from ecological restoration in myriad ecosystems across multiple scales. Establishing marine protected areas to help fish populations recover from exploitation leads to increased fish biomass, more catch per unit effort for fisheries, and increased tourism opportunities (Worm et al., 2006), which provides hope that passive restoration can be an effective tool to repair ocean fisheries while simultaneously providing cultural ecosystem services. Mangrove reforestation around Bangladesh has increased fishery potential, provided 600,000 m3 in forest products, bolstered livelihoods, and stabilized coastal land (Moberg and Ro¨nnba¨ck, 2003). The US Mississippi Delta provides $12–47 billion per year in flood and hurricane protection, water supply, water quality, recreation, and fishery ecosystem services (Batker et al., 2010). Moreover, if levees along the Delta were replaced with restored wetlands, there would be an estimated net gain of $62 billion in ecosystem services annually (Batker et al., 2010). Each of these studies illustrates the enormous potential for ecosystem service restoration in diverse ecosystems throughout the globe.

Using Ecosystem Services as Justification for Restoration One of the biggest utilities of ecosystem services in ecological restoration is as a justification to carry out restoration projects. In a resource and capacity-limited society, it is increasingly important that restoration projects make the case to society on their worth. Monetary justification is in sharp contrast to the moral justifications Aldo Leopold so vividly articulated in his Land Ethic (Leopold, 1949). While Leopold might disagree with the means, he would undoubtedly approve of the outcome of using ecosystem services to justify restoration because it shows society how connected to nature people are and speaks to society in a currency that everyone understands and appreciates. This is a modern way to help people understand their dependence on nature and bring even those living in industrialized cities (who use the majority of ecosystem services) a little bit closer to the land. The overwhelming majority of projects that interweave restoration with ecosystem services are in the developing stages and use ecosystem services to calculate the projected benefits of the proposed restoration (e.g., Loomis et al., 2000; Tong et al., 2007; Yu et al., 2009; Batker et al., 2010). For example, one study was done on the benefits of restoring the historical

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floodplains along the lower Danube River in Europe. Historical floodplains were converted to dykes for agriculture, aquaculture, and forestry, which reduced the capacity of the floodplain to absorb floodwaters and has increased flood peaks and spurred interest in restoration. The study showed that restored floodplains would provide $700 per hectare in flood control, provision of fish, forestry, and animal fodder, nutrient retention, and recreational benefits. In this case, projected ecosystem service benefits were two-fold higher than the cost of restoring this huge swath of land, which makes a strong case for investing in restoration (Ebert et al., 2009). Another study valued coastal wetlands for a single ecosystem service – storm protection – over the entire US. The authors determined wetland value by calculating the amount of storm damage in places with varying degrees of wetland protection and found that a loss of just one hectare of wetlands cost on average $33,000 dollars in hurricane damage. US wetlands currently provide $23.2 billion annually in storm protection and while no restoration costs were calculated, the study concludes that restoring wetlands is an extremely cost-effective strategy (Costanza et al., 2008). This massive ecosystem service value of coastal wetlands would be even higher if additional ecosystem services such as water filtration, toxin filtration, carbon sequestration, nursery habitat for commercially important fish, and recreational and tourism opportunities were included. This underscores the massive potential for large-scale restoration efforts to provide society with tangible benefits and preserve biodiversity in a single action.

Using Ecosystem Services as Explicit Restoration Targets Billions of dollars are spent annually restoring ecosystems (Enserink, 1999; Zhang et al., 2000), but with little to no consideration of the ecosystem service returns on the restoration investments (but see Goldstein et al., 2008). With so much money invested into restoring ecosystems, it is puzzling that so few restoration actions are prioritized according to the ecosystem services they can provide. As these two rapidly emerging fields continue to develop and expand, there will undoubtedly be growing numbers of restoration projects with specific ecosystem service goals, or projects that are prioritized by the amount of services they are likely to produce. Most restoration projects have a whole suite of ecosystem service benefits (Benayas et al., 2009). However, a key area for theoretical advancement is looking at the trade-offs between ecosystem services that specific restoration actions would entail. For example, reforesting an area that has been used as cropland will take away the food provisioning that the crops provide but may reinstate key water purification, flood protection, and carbon sequestration services. Studying these synergies and how they interact to restore ecosystems and contribute to human well-being will likely be one of the cutting-edge applications of ecosystem service restoration in the future.

The Future of Restoration and Ecosystem Services Tackling the Biodiversity Crisis Opinions differ on how best to stem the enormous biodiversity crisis that we face. The traditional conservation

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approach has been to preserve ‘‘natural’’ ecosystems by excluding people (Mittermeier et al., 1998; Reid, 1998; Holl and Aide, 2011). Inherent in this approach is the idea that people and ecosystems are separate entities – that humans are not part of nature. The growing consensus is that this viewpoint is antiquated, often produces maladapted conservation outcomes that may be difficult to maintain in perpetuity, and encourages conservation of nature at the expense of people (McNeely, 1994; Holling, 1996; Berkes, 2004; Kareiva and Marvier, 2011). While conserving biodiversity will continue to be an important strategy moving forward, doing so at the expense of people may ostracize man from nature and hinder conservation objectives. Restoring the earth’s damaged ecosystem services is one way to entwine two important objectives: Protecting and preserving biodiversity and providing the necessary functions and services for human survival. This is a unique way to reconnect people with nature and to simultaneously justify the need for restoring the damage we have inflicted. This is a relatively new way to engage society into conservation objectives and it has much progress ahead of it to ensure that it continues to be an effective conservation strategy. Even so, this is an exciting time to be a restoration ecologist. Restoration ecology is and will continue to be one of the most important sciences of the twenty-first century because of the widespread need to repair ecosystems globally. Society has placed great hopes on the ability of restoration to repair Earth’s damaged ecosystems and ensure continued survival for future generations (Palmer and Filoso, 2009). This is enormous pressure for such a nascent science but we are equal to the challenge. As restoration ecology continues to incorporate ecosystem services into its frameworks, there are important areas of research that will help to ensure that restoration is operational as a science but also meets society’s needs.

Key Challenges Many studies calculate ecosystem service benefits of conservation, restoration, or management projects. But very few of these examples examine the trade-offs and synergies of different ecosystem service benefits and so it remains difficult to predict how different restoration actions will affect ecosystem services as a whole. To understand these trade-offs, we must gain better understandings of how underlying ecosystem processes change with different restoration options and how ecosystem services change as a result (Palmer and Filoso, 2009). Right now, there are few satisfactory ways to value nonuse ecosystem services such as aesthetic values and so cultural ecosystem services are rarely valued (Portney, 1994; Benayas et al., 2009). Even indirect use (nonmarket) services can be valued in so many different ways (Pearce, 1993) that it becomes difficult to determine the accuracy of different valuation studies without intimate knowledge of economic theory. While this will continue to be a challenge for restoring ecosystem services going forward, it is also a prime opportunity to expand our existing theories and develop them to meet society’s needs. The interactions between ecological restoration, ecosystem service valuation, and climate change present enormous

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opportunities for further research. Discussions on climate change and ecological restoration are mostly theoretical (Harris et al., 2006), so there is ample opportunity for empirical studies to inform the discussion. Relatively more attention has been given to the effects of climate change on ecosystem services (Schroter et al., 2005), but there is still a dearth of studies that combine restoration, climate change, and ecosystem services. For example, it will be important to prioritize restoration efforts that help people adapt to climate change but it is unclear which restoration efforts will have the greatest adaptation benefits to people (Jones et al., 2012). Restoring coastal wetlands may be one of the most efficient and economical ways to protect people from sea-level rise and tropical storms (Costanza et al., 2008), but more research is needed to analyze the costs, benefits, and trade-offs of such restoration programs. Other areas may not be worth investing in restoring if they will be inundated by sea-level rise or destroyed by changing temperature regimes. Some species or ecosystems may not be resilient to projected climate change and therefore may be precluded from restoration investment, and others may thrive under climate change scenarios so they may be sought out as restoration targets. Empirical research is needed to examine different scenarios so that we can best prioritize our restoration actions in a changing world.

Integrating Restoration Goals with Societal Values Society is at a crossroads. We can continue to exploit Earth’s ecosystems with little thought to the effects it might have on other species or even future generations of our own species. We can unsustainably exploit resources and leave a legacy of extinction and degradation to future generations. Or we can recognize that our actions are not without consequence, take responsibility for those consequences, and begin making the difficult decisions that are necessary to ensure that future generations will have access to the food, clean water, timber, shelter, and other ecosystem services we all enjoy. Undoubtedly we have damaged ecosystems globally, but we do have the ability to repair damage, restore ecosystems, and ensure ecosystems can continue to provide the services that we all depend on for survival. This may require a large investment in restoration projects, a commitment to scientific research, and a change in our perception of our relationship with nature. But even in its infancy, restoration of ecosystem services can show society how much we stand to gain by making these changes. Using ecosystem service valuation to justify ecological restoration is just one way to reconnect people with nature and to start making more sustainable choices. In current society, it is also arguably the most salient one – the time to try to convince humanity that it is our moral duty to live in balance with the Earth has passed; it is now time to frame the imperative to restore differently, so that it speaks to everyone rather than a selected few. Making the economic case for restoration will be challenging going forward – ecosystem service valuation and ecological restoration still have much progress ahead of them. This is daunting because it is difficult to join two constantly changing disciplines, but it is also promising because they can both be developed alongside one another to leave them poised to

address the profound issues that our society faces. Restoration goals must be explicit, achievable, and take into account the varying views of ecosystems, societal expectations, and the dynamic nature of ecosystems. As we increasingly accept that invasive species, climate change, and unprecedented land transformation will produce novel ecosystems and species combinations never before seen, restoration may have to be directed toward some new system as opposed to a historical baseline (Marris, 2011). Restoration ecology is one science where creativity is necessary, along with scientific intellect, to achieve goals. Incorporating ecosystem services into restoration will require even more careful thought, ingenuity, and creativity. As these fields grow and expand, they will continue to push the boundaries of restoration to what might currently seem impossible. This progress will certainly be necessary in the face of an ever-growing human population, constant global change, and continued stress on the ecosystems that we depend on for survival.

Appendix List of Courses 1. Restoration Ecology 2. Biodiversity Conservation 3. Ecological Economics

See also: Biodiversity and Cultural Ecosystem Services. Priority Setting for Biodiversity and Ecosystem Services. Restoration of Biodiversity, Overview. Valuing Ecosystem Services. Wetland Creation and Restoration

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