Ecological Engineering 99 (2017) 486–495

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Ecosystem services must tackle anthropized ecosystems and ecological engineering S. Barot a,∗ , L. Yé b , L. Abbadie a , M. Blouin c , N. Frascaria d a

IEES-P, UMR 7618 (CNRS, INRA, UPMC, IRD), CC 237, 4 Place Jussieu, 75252 Paris Cedex 05, France CUP-Dédougou (Université de Ouagadougou), LERF, IDR, Université Polytechnique de, Bobo-Dioulasso, Burkina Faso Agroécologie, AgroSup Dijon, INRA, Univ. Bourgogne Franche-Comté, 26 Bd Docteur Petitjean, BP 87999, 21079 Dijon Cedex, France d Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91400 Orsay, France b c

a r t i c l e

i n f o

Article history: Received 23 November 2015 Received in revised form 20 November 2016 Accepted 21 November 2016 Keywords: Ecosystem services Disservices Anthropized ecosystems Ecosystem functioning Agroecology Ecological engineering Nature-based solution Sustainability Natural capital

a b s t r a c t The notion of ecosystem service is meant to better link human societies to ecological systems and to serve has a tool for decision making. However, the notion has never been applied in a comprehensive and consistent way to anthropized ecosystems while most ecosystems are indeed anthropized. This means that in initiatives of ecosystem service assessment anthropized ecosystems are either neglected or their services assessed in a misleading way. For example, services from cultivated lands are usually valued through the value of the agricultural production, while this production highly depends on inputs (fertilizers, pesticides, non-renewable sources of energy) and human work that cannot be assimilated to ecological factors. Moreover, these practices have negative impacts such as the emission of greenhouse gases, nutrient leaching to other ecosystems or loss of soil fertility. Hence, we present here a general framework that could be used to assess the ecosystem services provided by anthropized ecosystems. This framework is based on the joint assessment of ecological services, disservices, losses of natural capital and impacts on other ecosystems. We show that this framework is required to assess different practices to manipulate an ecosystem, e.g. low- vs high-input agriculture, or different ecosystems with different levels of anthropization, e.g. manage forest vs. cropland. Indeed, ecosystems function in such a complex way that human manipulations and natural ecological processes are tightly intermingled so that services and disservices arising solely from ecological processes cannot be separated from the result of human manipulations. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Ecosystem services are now defined as “the benefits human populations derive, directly or indirectly, from ecosystem functions” (Costanza et al., 1997) or “the benefits people obtain from ecosystems” (MEA, 2005). However, ecosystem services have already a long history (Gómez-Baggethun et al., 2010). The concept has initially been developed in the 1970s to support efforts of conservationists (Ehrlich and Mooney, 1983) and was thus used to raise stakeholder awareness on the pervasive negative impacts of human societies on biodiversity. Indeed, the concept of ecosystem service express the idea that human societies closely depend on natural ecosystems and the organisms they host. Hence, ideally, to convince that an ecosystem or organisms must be protected conservation-

∗ Corresponding author. E-mail address: [email protected] (S. Barot). http://dx.doi.org/10.1016/j.ecoleng.2016.11.071 0925-8574/© 2016 Elsevier B.V. All rights reserved.

ists just have to show that the ecosystem services they provide are very important for human societies. However, the mainstreaming of ecosystem services during the 1990s goes much further than a metaphor for the broad dependence of human societies on ecosystems. It leads now to technics of economic valuation of services. This allows building tools such as Payment for Ecosystem Services or Market for Ecosystem Services that put services very high on the political and economic agenda. Though these practices have also been criticized (Laurans et al., 2013; Silvertown, 2015), this means that ecosystem services are more and more viewed has an operational and pragmatic tool to help managing ecosystems. However, it seems that the current framework developed for ecosystem services has never been fully adapted to anthropized and managed ecosystems. The most classical definitions of ecosystem services (see above) do not give any precision on the type of ecosystem/level of artificialization that is acceptable for an ecosystem to provide ecosystem services. It is thus not fully clear whether ecosystem services can

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be assessed for anthropized ecosystems and, if so, there is so far no consensus on the way to assess ecosystem services provided by anthropized ecosystems. For example, a recent review has shown that the concept of ecosystems services has poorly been appropriated by agriculture sciences (Tancoigne et al., 2014). Indeed, since the original main goal was to push towards conservation the framework has originally been applied to ecosystems considered as natural. Some authors suggest that the notion of provisioning services (e.g. food production) can only be applied to rather natural ecosystems (de Groot et al., 2002) but nothing is explained about how croplands should be tackled. Similarly, in the global assessment of the value of ecosystem services (Costanza et al., 1997) nothing is specified about the way anthropized ecosystems are taken into account. For example, rangelands and crop lands provide provisioning services (i.e. food production) but the way these services were assessed is not clear. More recently, cultivated and urban areas have been explicitly excluded from another global assessment (de Groot et al., 2012) because they are human-dominated ecosystems. Nevertheless, some indicators of services or assessment methods have been proposed for anthropized ecosystems. For example Maes et al. (2012) map the service of water purification taking into account crop lands but do not map the provision services provided by the same agro-ecosystems. Other authors describe and discuss services provided by highly anthropized ecosystems such as urban areas (Bolund and Hunhammar, 1999; Gómez-Baggethun and Barton, 2013), crop lands (Maes et al., 2016) or totally artificial ecosystems such as green roofs (Oberndorfer et al., 2007), but without discussing the issue that in such ecosystems the provided services are also due to non-ecological processes (human work, inputs). In the same vein, in a comprehensive assessment of UK ecosystem services aiming at providing a guide to decision making all services were assessed together and services provided by agriculture were directly assessed using food market values (Bateman et al., 2013). Others acknowledge the problem of assessing ecosystem services that are provided by interactions between ecological systems and human work and non-natural capital but without giving clear solution (Heink et al., 2016; MAES, 2014). Our first goal is here to enlarge the current framework of ecosystem services to take into account anthropized ecosystems and all types of ecosystem manipulation by humans. This objective appears to us as crucial because all ecosystems are more or less impacted by human activities (Vitousek et al., 1997b). On the one hand, humans impact all ecosystems more or less directly without any conscious will. Even tropical primary forests have been modified by human groups inhabiting them (e.g. Posey, 1985) and are impacted by global changes triggered by human societies. Even Antarctic and Artic areas are touched by different forms of pollution (e.g. Weber and Goerke, 2003) and by climatic changes. On the other hand, about a third of earth terrestrial surfaces are utilized more or less intensively by humans for agriculture (Foley et al., 2011) and the original natural ecosystems have been purposely turned into cropping systems and pastures. This means that the framework for the assessment of ecosystem services is not fully adapted for the majority of ecosystems and may lead to misleading conclusions when applied to managed ecosystems such as crop lands, especially when different ecosystems with different intensity of anthropization or different types of management are compared. Ecological engineering is traditionally defined as “the design of sustainable ecosystems that integrate human society with its natural environment for the benefit of both” (Mitsch and Jørgensen, 2003). Our second goal is to better link the idea of ecosystem services to the field of ecological engineering (Barot et al., 2012; Mitsch and Jørgensen, 2003) and related types of ecosystem manipulations such as agricultural practices informed by ecological sciences (Altieri, 1989; Doré et al., 2011) or nature-based solutions

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(Eggermont et al., 2015). The framework of ecosystem services has originally been mostly applied to broad choices and issues. Which ecosystems should be protected? What surface of this ecosystem should be protected? The framework has more rarely been used to help making more refine decisions about ecosystem management and the underlying practices. This would allow answering questions such as: Which tree species should be planted in a street? What type of substrate should be used for a green roof? Should a cropping system be based on tillage? Should mixtures of varieties be used to develop a more sustainable agriculture? The framework we need should thus be able to compare in a comprehensive and consistent way the services provided by different ecosystems that may only differ by small differences in the practices used to manipulate the concerned ecosystems. This would in turn allow choosing the best practices to reach a particular goal defined as a targeted basket of ecosystem services. We might thus want to choose (1) the best combination of substrate type and irrigation practices to maximize the capacity of a green roof to store carbon and regulate the emission of greenhouse gases without having any particular requirement in terms of storm water retention or (2) the best combination of wheat varieties and inputs (fertilizers and pesticides) to maintain a high yield even in dry years and conserve soil fertility. This means that the framework we need should also explicitly take into account human work and management practices to allow more sustainable practices depending less on human work and non-natural capital to be chosen (e.g. less irrigation for a green roof or less fertilizer and less pesticide in agriculture), even when they lead to lower provision of the targeted services. To reach these two goals we have built a new framework starting from the framework described by Villamagna et al. (2013) to which we add (Section 2) the management of ecosystem to increase the provision of some services and a more explicit relation between ecosystem state, ecosystem functioning and the provision of services. We show (Section 3) that in anthropized or managed ecosystems services as often assessed are not truly ecosystem services because they are not solely based on ecological processes. Then we explain (Section 4) why it is not possible to fully disentangle the part of ecosystem services that are based on ecological processes and the part that is based on human work and nonnatural capital. Finally, we explain (Section 5) how this framework can be used and how it is linked to the sustainability of the provision of services.

2. Better integrating ecosystem services, ecosystem functioning and the feedbacks with human societies Our framework (Fig. 1) is based on the “capacity, flow, demand, pressure” framework (Villamagna et al., 2013). Note that we focus here on the capacity of ecosystems to provide services and not on interactions between this capacity and the demand by the society that lead to the actual flow of service. We emphasize that the capacity of provision of services (and disservices) is determined by a feedback loop between the ecosystem state (and its biodiversity) and ecosystem functioning and that this feedback loop is impacted by human activities. Very often this unintentional impact, i.e. pressure, is viewed as negative because many human activities alter the functioning of natural ecosystem (Vitousek et al., 1997b), e.g. through losses of biodiversity. However, human activities also often aim purposely at managing ecosystems or at increasing the provision of some services, i.e. agriculture aims at increasing food production. By definition, ecosystem services and disservices influence human societies (Fig. 1, arrows between services and human societies) and society should adapt their pressures on ecosystems and management practices according to their impact on the provision of services and disservices. This expresses the major objectives

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Fig. 1. Framework linking local ecosystem functioning, ecosystem services and the management of ecosystems. The diagram is based on the “Capacity, Flow, Demand, Pressure” framework (Villamagna et al., 2013). The actual flow of ecosystem services depends on the interaction between ecosystem capacity to provide services and the demand from the society. Here we emphasize that: (1) ecosystem functioning must be distinguished from services that directly benefit human societies, (2) the capacity to provide services depends on a complex feedback loop between the ecosystem state and biodiversity (the natural capital) and ecosystem functioning, (3) this feedback loop (and thus the capacity to provide services) is impacted by pressures, i.e. side effects of human activities or pressures linked to the functioning of other ecosystems or global changes, or by management practices that may purposely aim to improve the provision of particular services, (4) human societies should adapt the way they manage ecosystems depending on the ecosystem services and disservices they provide and the way management affect this provision.

of the notion of ecosystem services: making explicit the benefits human societies derive from ecosystems and triggering changes in the way we treat and manage ecosystems through the assessment of these benefits. More generally, and with the goal to include anthropized ecosystems and ecological engineering within the framework of ecosystem services, this means that human societies or ecological engineers should modify management practices and engineering methods, progressively and in an adaptive way (Schreiber et al., 2004). This should allow reaching particular goals defined as particular combinations of services and disservices. In agreement with Wallace (2007) and with reference to Fig. 1, we prefer to use the notion of ecosystem function than the notion of supporting service to restrict the use of the term of service to end-product services. (1) This approach avoids counting two times the same service; (2) It allows using the same term for all ecosystem processes or mechanisms whether there are viewed as leading to services (or disservices) or not; (3) All ecosystem functions are in close interaction and the resulting network of interactions leads (in a complex non-linear and hard to predict way) to ecosystem properties some of which can be considered services or disservices. Consequently, saying that a given ecosystem function is a service might be misleading because the function in itself might have positive or negative consequences for human societies depending on the context. For example, mineralization of dead organic matter is essential to ecosystem functioning. Clearly, without mineralization primary production would stop and ecosystems would crash down. However, increasing mineralization can also increase mineral nutrient losses from terrestrial ecosystems through leaching (Dijkstra et al., 2006), which should eventually decrease primary production of these ecosystems and may lead to eutrophication in aquatic ecosystems that receive the nutrients (Smith and Schindler, 2009). Moreover, increasing mineralization decreases the stock of dead organic matter (in soils and sediments), which releases CO2 , which likely increases the current global warming (Lal, 2004): in this case mineralization may be seen as decreasing the regulation services provided by ecosystems. At last, an ecosystem function that provides services in a given context may just be disconnected from services in other contexts. For example, mineralization may be viewed as allowing plant growth and subsequently berry production in a forest used by humans: the forest provides a provision service. However, this link to an ecosystem service is lost if humans never enter in this forest and therefore cannot eat the berries (the

forest has the capacity to provide a service but there is actually no flow of the corresponding service, Fig. 1). Thus, saying in a general way that mineralization is a service appears as nonsense. Overall, separating services from ecosystem functioning also allows emphasizing the complexity of ecosystem functioning and the difficulty to predict services from functioning (Escobedo et al., 2011; Norgaard, 2010). This also emphasizes that (1) studying the capacity of ecosystem to provide ecosystem services requires scientists specialized in ecology to study ecosystem functioning and the links between this functioning and services, (2) studying the flow of services and the way assessing services can be used to improve management requires economists and social scientists. Nevertheless, assessing the dependence of the provision of a service on a particular ecological function, as already done for pollination (Gallai et al., 2009), is a necessary approach to assess the importance of many ecological functions for human societies. Indeed, saying of an ecosystem process that it is a function, and not a service, does not depreciate this function. It is also important to assess disservices (Fig. 1) and focusing only on services could be misleading (Dunn, 2010; Heink et al., 2016). In particular: (1) only focusing on benefits provided by ecosystems is likely to bias our general vision of the relation between human societies and ecosystems because indeed ecosystems, either natural or anthropized, also lead to disservices. (2) It could be argued that disservices can be accounted for as negative amounts of services that can be subtracted from the quantified services. However, this is only a part of the story. For example, the leaching of mineral nutrients from an agro-ecosystem can be viewed as a decrease in a service of regulation (regulation of nutrient cycling or water purification). Nevertheless, the leached nutrients may end up in lakes or coastal areas that get eutrophicated (Smith and Schindler, 2009; Tilman et al., 2001). Because eutrophication impacts negatively many aspects of ecosystems (e.g. biodiversity, nutrient and carbon cycling), it is then more straightforward to consider the leaching of nutrients as leading to various disservices than as a decrease in a single service or regulation. (3) Many disservices are caused by the way ecosystems are manipulated, which may lead to original disservices. For example, the intensive use of pesticides in agriculture may lead to water pollution (see the discussion on this point next section). Note, that contrarily to Zhang et al. (2007) and as for services (see above) we only consider disservices as endpoints and not as intermediate ecological processes. Thus, pests that may decrease

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the yield of a field are counted as characteristics of the inner functioning of the field and not as disservices to the field functioning. Again, complex interactions between various ecological processes (e.g. food web dynamics, nutrient cycling) determine the ultimate impact of these pests on the provisioning services provided by the field.

3. Services, as currently assessed, are not fully produced by ecosystem functioning Ecosystem services have originally been defined (see Introduction) without mentioning anything about cases where ecosystems are impacted by human activities or purposely manipulated by humans. In cases where human influence is diffuse, for example when the functioning of an ecosystem is modified by species that have been introduced by human activities, this definition is likely to remain relevant. Indeed, in such cases, services are still provided, though in an altered way, by the mere functioning of the ecosystem, ecological processes and resources (e.g. organic matter, mineral nutrients, light, and water) that naturally flow within and between ecosystems. On the contrary, many ecosystems have been profoundly transformed so that their functioning and their mere structure have totally changed. This is particularly the case for artificial ecosystems that have been created by human activities such as cultivated areas, artificial lakes, artificial forests, urban green spaces or green roofs. If artificialization has mostly involved an initial manipulation and if ecosystems have then followed their own dynamics the general definition of ecosystem services still applies: even if the ecosystem is totally man-made the provided services are really provided by ecological processes. On the contrary, some ecosystems are created to provide particular services and the provision of these services highly depends on human manipulations that must be maintained or repeated on the long term. This is the case for agriculture (that we use here as our main example), cattle breeding or aquaculture. Particularly, if the provision of services, here provisioning services, relies on the constant use of inputs the definition of ecosystem services unlikely applies (see Fig. 2). The most obvious example is modern high-input agriculture. Such agriculture leads to high yields that have been multiplied by more than two in 50 years (Tilman et al., 2002). These yields are obtained and can be maintained for years, but only because: (1) the exportation of crops is compensated by the applications of huge quantities of fertilizer, (2) water may be provided to maintain production in unfavorable climatic conditions (irrigation), (3) pesticides are applied with high rates to make up for crop lack of defense against pathogens and herbivores and crop low competition ability against weeds, (4) mechanization requires the use of sources of energy not directly based on ecological processes (mostly fossil fuels). In such agricultural systems crops need soil, light and water to grow. They thus rely on some ecological universal processes (photosynthesis, uptake of water and mineral nutrients). However, it cannot be asserted that the yield is solely due to ecological processes. Consequently the whole yield cannot be fully considered as a provisioning service. The problem is that human manipulations and the related inputs have often non-desired effect besides increasing the provision of services and this likely leads to the non-sustainability of the provision of services (Fig. 2): (1) The required inputs are often produced in a non-sustainable way. (2) Manipulations may impact negatively the state of the managed ecosystem and its biodiversity, which may impair the future capacity of the ecosystem to provide services. (3) Human manipulations in interaction with ecological processes may lead to disservices. (4) Human manipulations in a managed ecosystem may directly or indirectly impact other ecosystems, which may

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lead to the provision of disservices in these ecosystems. These four points are explained below using agricultural examples. Nitrogen fertilization is based on the industrial fixation of atmospheric N2 that requires a lot of energy that is usually provided by fossil fuel combustion (Bøckman, 1997). Phosphorus fertilization is based on the exploitation of phosphate mines that will eventually get exhausted (Cordell et al., 2009). Irrigation is based on the use of a resource that is naturally circulating but this resource must be artificially gathered and transferred to the agro-ecosystems and it is then no longer available to other natural ecosystems. Pesticides are synthesized industrially, which has a cost in terms of energy and the necessary raw materials. Modern agriculture is based on mechanization which requires the use of fossil fuels. In all these cases, the production of inputs and their use is not sustainable. Ecosystem manipulations may increase the provision of services on the short-term while impacting negatively the ecological state of the ecosystem and its biodiversity, which may decrease the long-term capacity of the ecosystem to provide services: these processes correspond to losses of natural capital (Costanza and Daly, 1992). The natural capital is thus the state of ecosystems that underpins their capacity to provide services and the losses of natural capital should be taken into account when assessing ecosystem services. We might think, for example, that a service produced under the deterioration of an ecosystem cannot be considered an ecosystem service. At least, we should decide to assess the costs in terms of the future decrease in the provision of ecosystem services together with the present provision of ecosystem services. For example, in agriculture, high yields are often obtained through losses of soil fertility (e.g. erosion, loss of mineral nutrient, loss of organic matter, deterioration of soil structure) and losses of soil biodiversity and biomasses (macrofauna, micro-organisms). This corresponds to long term trends that have been exacerbated by modern intensive agriculture. This has led to the degradation of 40% of cultivable lands and 6% of these lands have been so much degraded that the restoration of their fertility is nearly impossible or would require very high investments (Oldeman et al., 1994). Fisheries are also a good example of decrease in natural capital. Intensive fishing depletes fish populations, which often decreases the capacity of these populations to reproduce and produce the biomass that can be harvested in the near future (Hutchings, 2000). Similarly, fishing and other human activities (e.g. through pollution, global changes) have often impacted negatively the functioning of the ecosystems on which fisheries are based (Murawski, 2000). Again, this decreases the capacity of oceans to produce fishes and the corresponding provisioning services. Both the use of fertilizers and pesticides lead to negative ecological consequences, i.e. disservices provided by the local managed ecosystem. Indeed, an important proportion of fertilizer and pesticides is leached out of agro-ecosystems. Agricultural practices can also increase the release of greenhouse gases (CO2 due to the mineralization of soil organic matter, N2 O due to denitrification). Pesticides may both impact non-targeted organisms within agroecosystems and cause serious health problem for humans. Local human manipulations of ecosystems may also have impacts at wider scales. The production of inputs may directly impact ecosystems and the biosphere. For example, the use of fossil fuels contributes to climate changes. Depending on local ecological processes, manipulation of a local ecosystem may also impact other ecosystems (Fig. 2). For example, depending on the capacity of agro-ecosystems to regulate nitrogen and phosphorus fluxes, the wide use of fertilizers strongly contributes to the global enrichment of ecosystems in nitrogen and phosphorus (Cordell et al., 2009; Vitousek et al., 1997a), which leads for example to the eutrophication of many aquatic ecosystems. Pesticides may be leached out of agro-ecosystems and may impact organisms living outside agro-ecosystems and the functioning of their ecosystems (Mottes

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Fig. 2. Framework to assess ecosystem services provided by anthropized ecosystems. In addition to the (1) services themselves (partially due to ecosystem manipulations and inputs), we should assess (in red): (2) disservices (partially due ecosystem manipulations and inputs), (3) changes in the state and functioning of the ecosystem that impact the future provision of services (i.e. variations in the natural capital), and (4) the sustainability of the production of the inputs used, (5) impacts of ecosystem management that impact directly or indirectly other ecosystems and the disservices they provide. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

et al., 2013), particularly aquatic ecosystems. Both eutrophication and contamination by pesticides thus impact the functioning of ecosystems (outside of agro-ecosystems) and may thus alter the disservices and services they provide. 4. Ecological mechanisms and human manipulations are too intricate to be disentangled Fig. 3 and the above arguments (see preceding section and Fig. 2) show that when ecosystems are manipulated a part of the services they provide are not truly ecosystem services. Ideally, when services are assessed the “true ecosystem services” that arise from ecological processes and the services arising due to human manipulations should be evaluated separately. However, this is in most cases not possible. Indeed, as we argue above (comments linked to Fig. 2), ecosystem functioning is the result of a network of ecological interactions involving many species, abiotic factors, ecological mechanisms, manipulations by humans and feedbacks at various temporal and spatial scales. These manipulations are closely tangled with the whole network of interactions, which cascades on ecosystem services and disservices in a complex way. Consequently, the resulting provision of various ecosystem services cannot be attributed to ecosystem processes per se or to manipulations and inputs per se. For example, in a field all the yield is based on photosynthesis and could be considered as an ecosystem service for this reason, but the whole yield is also based on sowing and the related inputs (e.g. at least fuel for the tractor), which suggests that the yield cannot be considered at all as an ecosystem service. Removing either photosynthesis or sowing reduces the yield to zero so that it is not possible to assess the percentage of the yield that is due to sowing. Examining more refine mechanisms leads to the same type of conclusion. For example, the increase in cereal production since the 1960’s is highly linked to the increasing use of nitrogen fertilizers (Tilman et al., 2001), which suggests that cereal production is less and less an ecosystem service. However, the mean residence time of nitrogen fertilizers is several decades (Sebilo et al., 2013). Though a part of fertilizers is quickly leached, a significant fraction is incorporated in soil organic matter and

recycled several times before being taken up by the crop or being leached. This means that the yield is significantly impacted by all ecological processes governing soil capacity to retain nitrogen, e.g. processes that determine the capacity of soil microorganisms to immobilize and release nitrogen. Thus, even the impact of mineral fertilization on yield depends on ecological processes so that the yield can be considered partially as an ecosystem service. As for services, it is impossible to separate disservices that arise due to natural ecosystem functioning and to manipulations by humans (Fig. 3). For example, pesticides and fertilizers lead to the pollution of continental waters, which leads to various disservices (see above). Intricate interactions between the manipulation and natural ecological processes determine the quantity of pesticides and fertilizer that is leached out of the field. For example, the dynamics of pesticides within the soil should depend on the pesticide used and the way it is spread but also on soil properties, its texture, its content in organic matter and the activity of its microorganisms (Bailey and White, 1970). Thus, pollution by pesticides also depends on ecological processes. Conversely, the emission of allergens by vegetation can be viewed as a true disservices arising solely due to ecological mechanisms. However, as soon as vegetation is managed, for example in agriculture, the emission of allergens should also be influenced by human manipulations. Hence, it is not possible to strictly separate true disservices that would only arise due to ecological mechanisms from disservices that only arise due to human manipulations. Note that an other argument for considering the impacts of human manipulations of ecosystems that feedback negatively to human societies as disservices is that symmetrically the positive impacts of these manipulations are already considered as services in the literature. These arguments show that to asses ecosystem services provided by an anthropized ecosystem the only comprehensive option would be to assess independently the manipulations and all their consequences as well as the services, (see Fig. 2): (1) the sustainability of the production of inputs, (2) modifications of the local ecosystem state, biodiversity and functioning that may decrease the future capacity of the ecosystem to provide services (gains or losses of natural capital), (3) disservices that are in fact an intricate

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Fig. 3. Diagram showing that ecosystem services are partially due to the way human societies manipulate ecosystems and affect their functioning. This means that these services are not only produced through ecological processes. They are also produced through inputs (e.g. fertilizers) that are usually not produced in a sustainable way. A Ideally, we should assess separately true ecosystem services produced through ecological processes (in blue), i.e. net ecosystem services, from services that are due to inputs (in red). B However, within ecosystems the effects of ecosystem management and ecological processes are so tightly interacting that it is only possible to measure the overall provision of services (in purple), i.e. gross ecosystem services. For the same reason, it could be useful to assess the net ecosystem disservices purely due to ecological processes but we only have a direct access to gross ecosystem disservices. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

mixture of true disservices (arising due to ecological processes) and negative environmental impacts arising due to human manipulations and inputs, (4) impacts on the biodiversity and functioning of other ecosystems, (5) changes in the services and disservices provided by other ecosystems, (6) services provided by the managed ecosystem that are in fact an intricate mixture of true services (arising due to ecological processes) and services arising due to human manipulations and inputs. Here, as others (Fisher et al., 2009) we argue that there is not a single solution for the assessment of ecosystem services. It is advisable, depending on the context and the objectives, to use different classifications of services and different ways to add up services and account for ecological costs. Nevertheless, the general idea to assess in a comprehensive and inclusive way ecosystem services of anthropized ecosystems would be to subtract the costs of inputs and manipulations (points 1 to 5 in the preceding paragraph) from the total ecosystem services (point 6), i.e. “gross ecosystem services”, to obtain the “net ecosystem services” (see Fig. 3). However, this is only possible if all quantities can be quantified using the same unit. It could be possible for example if all benefits and costs are converted into stocks and flow of carbon, or into a currency. However, this is not necessary possible (Jax et al., 2013; Norgaard, 2010; Silvertown, 2015) and we think that, in many cases, it is advisable not to try assessing the net ecosystem services but rather to asses jointly services and environmental impacts of ecosystem manipulations.

5. Consequences and utilization of the framework According to the above rationale, the best way to assess and compare different anthropized ecosystems and the underlying engineering is to examine jointly the provision of services, disservices and other negative consequences of human manipulations (see Fig. 2). The results can for example be displayed using a radar diagram (Fig. 4). For the sake of clarity, we have used here two contrasted examples, i.e. low- and high-input agricultures, to show that

no type of ecosystem manipulation is likely to be perfect, maximizing the provision of all types of services, leading to no disservice and being fully sustainable. Our framework should apply to any type of ecosystem and whatever the level of anthropization and manipulation of the ecosystem. Our framework is necessary in all initiatives based on the assessment of ecosystem services that need to compare ecosystems with different levels of anthropization and inputs. The framework would for example allow extending existing studies (e.g. de Groot et al., 2012) to all types of ecosystems or to improve the assessments that already take into account anthropized ecosystems such as agro-ecosystems (e.g. Bateman et al., 2013). Indeed it would be misleading to compare ecosystem services provided by a forest and a cropping system, or provided by two cropping systems with different levels of inputs without taking into account the negative impacts of human manipulations. The goal of the present article is not to give details on the methodology to assess services, disservices and negative impacts of ecosystem management (Fig. 5). Services and disservices can be assessed using standard up-to-date methodologies (Maes et al., 2012). Standard methods to assess disservices can be adapted to assess disservices that are particular to managed ecosystems (e.g. leaching of pesticides and fertilizers from a cropland) (Pretty et al., 2000). Changes in ecosystem state and biodiversity that threaten their capacity to provide services can be assessed using ad hoc indexes linking ecological functioning to its state. Such indexes have for example been developed for lakes (Xu et al., 2001) and soils (Schloter et al., 2003). The lack of sustainability of input production and negative impacts on other ecosystems can be assess using methods inspired by Life Cycle Assessment (Finnveden et al., 2009; Roy et al., 2009) and environmental impact assessment (Jay et al., 2007). This means that the general methodology for our approach already exists, but that applying the approach will require adjustments and building new lists of indicators. The framework could also be used to assess the capacity of any manipulation of an ecological system to provide services in a sustainable way (see Fig. 5). While ecological engineering is tra-

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Fig. 4. Comparison between two fictive ecosystems that provide different amounts of services, disservices and that are submitted to two contrasted types of manipulation: The first ecosystem corresponds to low-input agriculture or any type of ecosystem manipulation based on ecological engineering. The second ecosystem corresponds to high-input agriculture or any ecosystem whose management is based on non-natural capital. The diagram is not based on real data and has only a demonstrative value. The axis is based on an arbitrary common scale. Importantly, for services, changes in the ecosystem state, i.e. change in the natural capital, and the sustainability of the production of inputs the higher is the value the more favorable the ecosystem manipulation is, while for disservices it is the reverse.

Fig. 5. List of criterions that should be used to assess the sustainability of local ecosystem management and the sustainability of the subsequent provision of ecosystem services. These criterions are hierarchized according to the spatial scales involved (from the manipulated ecosystem to the biosphere) and according to the strictness of the criterion: indeed if the central criterions (in red) are not met there is no way the provision of services will last for ever. Local management practices can be maintained even if they lead to disservices or impact negatively the biodiversity and functioning of other ecosystems in the sense that these practices do not threaten the provision of services by the local ecosystem. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

ditionally defined without mentioning ecosystem services (Mitsch and Jørgensen, 2003), this is not necessarily the case (Barot et al., 2012). In our opinion, the link between ecological engineering and ecosystem services is obvious because the goal of ecological engineering is to manipulate ecosystems to provide services that should be “true ecosystem services”. In other words, in order to provide services, ecological engineering should increase the relative influence of ecological processes and functions on the provision of services (that we do not want to call supporting services, see Fig. 2), while decreasing the relative influence of inputs and human work and the subsequent negative effects. Ecological engineering and

ecosystem services are also linked by the idea of self-organization or self-design that has been emphasized by the founders of the field (Mitsch and Jørgensen, 2003; Odum and Odum, 2003). Indeed, that a manipulation of an ecological system relies on self-organization also means that it relies less on a repeated human intervention and inputs, and that it relies more on ecological processes. This, in turn, means that: (1) Services provided by self-organized ecological systems should be counted as true ecosystem services. (2) The manipulations of these systems are less based on the use of nonrenewable resources. (3) These manipulations increase rather than decrease the long term capacity of the ecosystem to provide services. (4) These manipulations do not lead to disservices. Note that agro-ecology can be defined in the same way as ecological engineering in the restricted domain of agriculture (Altieri, 1989; Barot et al., 2012). Our above rationale about ecological engineering thus perfectly applies to agro-ecology. Agro-ecology can be considered as aiming at increasing the provision of “true provisioning services” by agro-ecosystems. Ecological engineering, agro-ecology and nature-based solutions have been associated to the notion of sustainability right from the conception of these fields (Altieri, 1989; Eggermont et al., 2015; Mitsch, 2012; Mitsch and Jørgensen, 2003). Ecosystem services are also viewed as a boundary object that can be useful to foster sustainability (Abson et al., 2014). However, defining and assessing sustainability is a complex multi-dimensional and multi-scale task (Gibson, 2006; Moldan et al., 2012; Singh et al., 2009). Our framework is only relevant for the environmental pillar of sustainability and we more precisely focus on the sustainability of local practices of ecological engineering, i.e. on the ecological capacity of a managed or more or less anthropized ecosystem to provide services on the long-term. There has already been much debate on the way to assess sustainability, for example of agriculture (Rigby and Cáceres, 2001; Rigby et al., 2001; Struik et al., 2014), and there is so far no consensus. The list of general criterions we have chosen (Fig. 5) is in our opinion comprehensive. First of all, the management of the ecosystem should not modify the ecosystem (e.g. soil fertility or biodiversity) in a way that threatens the future provision of services (problem of agricultural practices decreasing soil fertility) and the inputs used for the ecosystem management should be produced in a sustainable way (problem of phosphorus fertilizer). If these two criterions are not met, the provision of services will necessarily have a limited duration. Then, the disservices provided by the manipulated ecosystem or triggered in other ecosystems by the ecosystem

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manipulation do not directly threaten the provision of services. However, from a wider scale perspective there is no point increasing the services provided by an ecosystem if it also highly increases the provision of disservices. Moreover, if these disservices correspond to regulation problems (e.g. production of greenhouse gases) these disservices will lead to sustainability problems at larger scales that the scale of the manipulated ecosystem (e.g. climate change). Finally, the manipulations of an ecosystem that negatively impact the functioning and the biodiversity of other ecosystems might not directly impact human societies. However, these manipulations likely play a role in the global lack of sustainability of the interactions between human societies and the biosphere. The problem is that management practices (e.g. agriculture) are often applied on huge areas, which has led many “planetary boundaries”’ to be crossed (Steffen et al., 2015). Taken together, our framework can help assessing sustainability but the goal cannot be to draw a precise border between manipulations of ecosystems that are sustainable and the ones that are not. The key point is that the less the criterions we list (Fig. 5) are met the less sustainable is the manipulation of the ecosystem and the subsequent provision of services. Importantly, this list of criterions is based on the realistic hypothesis of “strong sustainability”, i.e. that at least some aspects of the natural capital cannot be substituted by non-natural capital (Ekins et al., 2003). Overall, our framework allows comparing, in a comprehensive way, different practices of ecological engineering or agro-ecology and their sustainability. It also allows comparing these practices to more traditional practices. Others, like Kremen (2005), have advocated for an explicit management of ecosystem services but do not go as far as ecological engineering or engineering of ecosystem services, and they do not mention the necessity to account for the negative environmental impacts of this management. This would also be important for ecological engineering in very anthropized areas such as towns. For example, green roofs are thought to provide diverse ecosystem services (Oberndorfer et al., 2007) but these services depend on the way these roofs are managed and they may also provide disservices (e.g. release of greenhouse gases). Ideally, green roofs should be self-organized ecosystems that provide services without human intervention and the use of non-renewable resources. However, green roofs may require some maintenance (e.g. irrigation, fertilizers, mowing) and the construction of a green roof may also require inputs that are non-sustainably produced (at least due to the production of the substrate of the green roof or the use of fossil fuels as sources of energy).

6. Conclusion Our framework leads to state that ecological engineering (or any related type of practice related to nature-based solutions or agroecology) should consist in engineering technics, informed by ecological sciences, that allow reaching particular combinations of provisioning, regulation, cultural services, disservices, ecosystem state and that allow increasing the provision of services while decreasing the subsequent negative impacts. Describing the way particular combinations of services and disservices and other negative impacts should be targeted goes far beyond the objectives of our paper. These are fundamental but very complicated issue because the services, disservices and costs are linked in a complex way, which imposes trade-offs (Bennett et al., 2009; Chisholm, 2010; Power, 2010). Importantly, tackling thoroughly these issues in a comprehensive way requires more ecological researches on (1) the functioning of ecological systems, (2) their reactions to manipulations, (3) links between ecosystem functions and the provision of services and disservices, (4) constraints leading to tradeoffs between services. Tackling these issues also requires more

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researches in social sciences and economy to improve the way combinations of services, disservices and ecological costs are targeted and to determine how the corresponding manipulations/practices may be implemented within the actual socio-economical context. Agronomy has not waited for our framework to assess impacts and benefits of agriculture practices (Pimentel et al., 2005; Pretty et al., 2000; Tilman, 1999). More recent studies linking agriculture and ecosystem services mention the fact that disservices and negative environmental consequences of ecosystem manipulations have to be taken into account (Dale and Polasky, 2007; Swinton et al., 2007). But even some studies aiming at testing alternative agriculture strategies often focus on services and not on the negative impacts of human manipulations (Palm et al., 2014; Sandhu et al., 2010). In this context, our framework is new because it emphasizes the necessity to fully merge different fields that have so far developed partially independently: (1) assessment of ecosystem services and disservices, (2) assessment of impacts of human manipulations of ecosystems on human societies, (3) ecological engineering and all disciplines such as agroecology aiming at designing ways to manipulate ecological systems to reach particular goals. Finally, there is a relation between our framework to assess ecosystem services of anthropized ecosystems and the idea of alternatives to Gross National Product (GNP). Increasing inputs to agriculture increases the quantity/value of food produced and the quantity/value of inputs sold. This should thus trigger an increase in the GNP. However this also (1) decreases a non-renewable natural capital (P is exploited in mines), (2) might decrease soil C stock (loss of organic matter), (3) release CO2 (production of N fertilizers), (4) leads to leaching of N, P or pesticides to other ecosystems. Alternatives to GNP that better describe well-being and social and environmental impacts (Costanza et al., 2014) should emphasize the fact that many human activities (e.g. increasing agricultural yields using non-renewable resources and producing disservices) are not sustainable and likely decrease human wellbeing on the long run. Such alternative indexes should use net (or true) ecosystem services and not gross ecosystem services. Our tentative framework could probably be useful in this context. The notion of ecosystem service has spread successfully in many domains of the society and the economic life. However, groups of citizens and scientists object to this notion or at least to its wide and blind use to govern political and economic decisions (Jax et al., 2013; Silvertown, 2015). One broad criticism is that the present use of the notion of ecosystem services cannot help to amend the production system because this use is based on the present functioning of the economic system that can be viewed as the cause of the present environmental crisis (Gómez-Baggethun et al., 2010). This criticism could partially be alleviated using our more inclusive assessment of ecosystem services that count negatively the use of non-renewable inputs to produce services and all related environmental impacts of ecosystem manipulations. We argue in particular that assessing at the same time the benefits and negative impacts of ecosystem manipulations is necessary to avoid “rebound effects” (Maestre Andrés et al., 2012). This could for example arise if policies aim at increasing the provision of a given service without taking into account the subsequent provision of disservices or other negative environmental impacts. In turn, this should foster the development of alternative more sustainable practices in many domains of human activities.

Acknowledgments The content of this article is the fruit of various discussions that have been held within the Gaié group (Group of the Actors of Eco-

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logical Engineering). We thank the two reviewers for their valuable comments on our manuscript.

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