Original ArticlesWhat can indicators of good environmental status tell us about ecosystem services?: Reducing efforts and increasing cost-effectiveness by reapplying biodiversity indicator data
Introduction
Biodiversity is closely linked to ecosystem functioning, which in turn underpins the provision of ecosystem services on which humanity depends, such as Food provision and Climate regulation (Heiskanen et al., 2016, Liquete et al., 2016). According to the Convention on Biological Diversity (CBD, 1992), biodiversity is defined as “the variability among living organisms from all sources including, inter alia, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, between species and of ecosystems”. Yet, biodiversity is threatened worldwide by pressures such as habitat loss, overexploitation and pollution (Halpern et al., 2008, Knights et al., 2013). International environmental agreements, such as the Aichi Biodiversity Targets for 2020 in the Convention of Biological Diversity (CBD, 1992), the EU Biodiversity Strategy 2020 (BD; COM/2011/0244), and recent European Union legislation (e.g. the EU Marine Strategy Framework Directive (MSFD; 2008/56/EC)) are placing increasing emphasis on halting biodiversity loss (Laurila-Pant et al., 2015, Liquete et al., 2016).
The MSFD “establishes a framework for community action in the field of marine environmental policy”, which promotes the preservation and protection of marine waters in European member states (European Commission, 2008). One aim of the MSFD is for each member state to take measures to achieve and maintain Good Environmental Status (GES) in all four European Seas (i.e. Baltic Sea, Black Sea, Mediterranean and North East Atlantic) by the year 2020, through country-specific programmes of measures (Börger et al., 2016). The MSFD defines GES as: “the environmental status of marine waters where these provide ecologically diverse and dynamic oceans and seas which are clean, healthy and productive within their intrinsic conditions, and the use of the marine environment is at a level that is sustainable, thus safeguarding the potential for uses and activities by current and future generations.” This definition implies that ecosystem services and societal benefits should be taken into consideration when measuring GES but at the same time these aspects are not mentioned in either the descriptors or associated criteria (Borja et al., 2013). Recently, changes were suggested to some elements of the MSFD, including criteria and Annex III, these are now awaiting acceptance. Among these changes is the acknowledgement that member states may also assess ecosystem services under MSFD. These changes demonstrate the importance of comparing ecosystem service indicators and biodiversity-related indicators (from now on biodiversity indicators).
To assess the status of the seas and to be able to monitor changes in environmental status, each member state has to carry out regular assessments addressing 11 descriptors that describe a state, or a pressure, or both. These are: Descriptor (D) D1–Biological diversity, D2–Non-indigenous species (NIS), D3–Commercial fish and shellfish, D4–Food webs, D5–Eutrophication, D6–Sea floor integrity, D7–Hydrological conditions, D8–Concentration of contaminants, D9–Contaminants in fish and other seafood, D10–Litter, D11–Energy and noise. These 11 descriptors are further defined by a set of 29 criteria and 56 indicators. Indicators are variables that provide information on complex phenomena and if properly selected can show changes of such phenomena (Kandziora et al., 2013, Hattam et al., 2015). A requirement of the MSFD is that indicators focus on essential biological components of the ecosystem, from taxonomic groups through habitats to ecosystems (Borja et al., 2014, Berg et al., 2015). Member states considered the different criteria and indicators, and for those of relevance to their seas they defined a series of indicators to be used to describe a baseline, and then in regular monitoring programmes to assess the success of their programmes of measures.
The biological components relevant for biodiversity assessments are described by Cochrane et al. (2010), and specifically listed in Table 1 of the Annex III of the MSFD. The biodiversity components include predominant seabed and water column habitat types, as well as specific habitats that have biodiversity conservation importance. Biological communities associated with those seabed and water column habitats, such as phytoplankton and zooplankton communities, angiosperms, macro-algae and invertebrate bottom fauna, or species belonging to groups such as fish, marine mammals and reptiles, and seabirds are also included in the biodiversity components. Currently there are a number of operational indicators available for the assessment of GES (Teixeira et al., 2016), and more are being developed to be used in robust and cost-efficient monitoring and assessments (Heiskanen et al., 2016).
Besides monitoring the status of marine waters, the MSFD dictates that member states shall adopt an ecosystem-based management approach in their programmes of measures to “enable the sustainable use of marine goods and services” (Paragraph 8 of the MSFD preamble). Ecosystem-based management is focused on ecosystems and human interactions within these systems, and thus necessitates an understanding of the linkages within and between the biological components of the ecosystems as well as with social and economic systems (McLeod et al., 2005, Atkins et al., 2011). Furthermore, it is stated in the MSFD Article 1, Paragraph 3.: “Marine strategies shall apply an ecosystem-based approach to the management of human activities, ensuring that the collective pressure of such activities is kept within levels compatible with the achievement of good environmental status and that the capacity of marine ecosystems to respond to human-induced changes is not compromised, while enabling the sustainable use of marine goods and services by present and future generation”. This anticipates that there is a link between GES and the sustainable use of ecosystem goods and services. Although many of the GES indicators are well described and used by EU member states, there is no operational example describing how these could also be used in the assessment of ecosystem services, although some regional (Hasler et al., 2016) and EU-level (Maes et al., 2016) suggestions have been made. Here we conceptualise ‘sustainable use’ in the sense of ‘weakly sustainable use’ (sensu Rossberg et al., 2017) i.e. usage that can be continued indefinitely in its current form. The key concept to assess status and trends of potential uses of an ecosystem, particularly relevant in local and regional settings, is that of ecosystem services (Maes et al., 2012, O'Higgins and Gilbert, 2014). Ecosystem services are the direct and indirect contributions of ecosystems to human well-being (TEEB, 2010) and are increasingly being considered in marine policy and planning (Fisher et al., 2009, Börger et al., 2014, Pendleton et al., 2016).
In the Millennium Ecosystem Assessment (MEA, 2005) ecosystem services were split into four groups: i. provisioning, such as food and timber; ii. regulating, for example regulating climate or water flows; iii. cultural, such as aesthetic experience derived from being in nature; and iv. supporting, for example supply of larval fish (in this example supporting the service of Food provision). This approach was criticised as it did not differentiate between processes and services or services and benefits, potentially leading to double counting (Fisher et al., 2008). Since then several alternative classifications have been proposed (Liquete et al., 2013), including a more hierarchical approach as defined by Fisher et al. (2009) which renamed the supporting services as intermediate services or processes. CICES (Common International Classification of Ecosystem Services) is another classification example, which merges regulating and supporting ecosystem services into a new category of “regulating and maintenance” ecosystem services and also includes a separate framework for abiotic services (Haines-Yong and Potschin, 2013). Within this study, seven ecosystem services (Table 1) were chosen that included examples from the MEA ecosystem service groups.
While the scientific literature on ecosystem services continues to grow it is still a challenge to apply this concept in practice (Kandziora et al., 2013). To assess ecosystem services, it is important to understand and quantify the link between biodiversity; i.e. species or communities or traits of species and the flow of services they supply or to which they contribute. However, this challenging task is hampered because biodiversity-ecosystem function relationships are still subject of ongoing research, particularly in the marine environment (Liquete et al., 2013, Gamfeldt et al., 2015, Strong et al., 2015). Yet, some biological components of the ecosystem do play clear roles in the provision of ecosystem services (Kandziora et al., 2013). For example, charismatic species attract visitors for ecotourism and therefore contribute to the service of Leisure and Recreation (Uyarra and Côté, 2007). In this way ecosystem services can be linked to MSFD biological components. Another example is the invasive macrozoobenthic polychaete genus Marenzelleria which, in the Baltic Sea, enhances retention of phosphorus in sediments and so promotes the Bioremediation of waste service (Norkko et al., 2012). Effects of biodiversity on ecosystem services may be explained by functional traits of species, so identification of “key functional traits,” that have the capacity to influence the provision of multiple ecosystem services, is promising (Hevia et al., 2017). Table 2 lists examples of how each component contributes to the provision of particular ecosystem services.
Links between ecosystem components and ecosystem services can help to identify suitable ecosystem service indicators. The biodiversity indicators used to monitor GES could then also be used to assess ecosystem services, providing a cost-effective approach to support the management of regional seas and the services they provide. Several ecosystem service indicator lists have been published although none claims to be complete (Böhnke-Henrichs et al., 2013, Liquete et al., 2013, European Commission, 2014, Atkins et al., 2015, Hattam et al., 2015). Currently there are no accepted operational practise nor guidelines for the development or selection of useful marine ecosystem service indicators (Hattam et al., 2015, Hasler et al., 2016). Therefore, in this study, we have considered the applicability of biodiversity indicators for assessing the seven selected marine ecosystem services, to support the practical application of ecosystem services as a management tool within the framework of the MSFD implementation or other biodiversity assessments.
Section snippets
Marine ecosystem service indicators
It was deemed efficient to concentrate on a broad selection of ecosystem services rather than all services, because each service indicator had to be cross checked against each biodiversity indicator, which is more manageable with a smaller number of services. This approach resulted in seven ecosystem services being selected for this study (MEA category in brackets): Food provision (provisioning), Climate regulation (regulating), Disturbance prevention and moderation (regulating), Bioremediation
Comparability of biodiversity and ecosystem service indicators
In total, of the 296 operational DEVOTOOL indicators, 64 were directly comparable to published ecosystem service indicators while 232 indicators were not (Fig. 1). Twenty indicators were useful for Food provision. Climate regulation could be measured with two indicators, Disturbance prevention with one, Bioremediation with eight and Biological control with eleven. Biodiversity indicators were most applicable for cultural services Leisure and recreation (35) and Aesthetic experience (30). Of
Discussion
This paper identifies potential indicators for seven selected ecosystem services from a list of biodiversity indicators prepared for the GES assessment of the MSFD. Ecosystem services are generated from many interactions in complex systems and not all links between ecosystem components and ecosystem services are fully understood (Balvanera et al., 2013, Liquete et al., 2016). For some services the role of the contributing components is clear. For others, relationships between ecosystem
Acknowledgements
Torsten Berg helped with some data extraction from DEVOTOOL and advised on technical issues and Susanna Jernberg helped to evaluate linkages of some Baltic Sea indicators with ecosystem services. The authors would also like to acknowledge DEVOTES (DEVelopment Of innovative Tools for under-standing marine biodiversity and assessing good Environmental Status) project funded by the European Union under the 7th Framework Program, ‘The Ocean for Tomorrow’ Theme (grant agreement no. 308392, //www.devotes-project.eu
References (54)
- et al.
Management of the marine environment: Integrating ecosystem services and societal benefits with the DPSIR framework in a systems approach
Mar. Pollut. Bull.
(2011) - et al.
Typology and indicators of ecosystem services for marine spatial planning and management
J. Environ. Manage.
(2013) - et al.
Incorporating ecosystem services in marine planning: the role of valuation
Mar. Policy
(2014) - et al.
The use of multiple biological traits in marine community ecology and its potential in ecological indicator development
Ecol. Indic.
(2017) - et al.
Good Environmental status of marine ecosystems: what is it and how do we know when we have attained it?
Mar. Pollut. Bull.
(2013) - et al.
The impact of tourism and personal leisure transport on coastal environments: a review
Estuar. Coast. Shelf Sci.
(2006) - et al.
Defining and classifying ecosystem services for decision making
Ecol. Econ.
(2009) - et al.
Marine ecosystem services: linking indicators to their classification
Ecol. Indic.
(2015) - et al.
A methodology for the assessment of local-scale changes in marine environmental benefits and its application
Ecosyst. Serv.
(2014) - et al.
Interactions of ecosystem properties, ecosystem integrity and ecosystem service indicators—a theoretical matrix exercise
Ecol. Indic.
(2013)
How to value biodiversity in environmental management?
Ecol. Indic.
Perspectives on the link between ecosystem services and biodiversity: the assessment of the nursery function
Ecol. Indic.
Quantifying and modelling the carbon sequestration capacity of seagrass meadows −A critical assessment
Mar. Pollut. Bull.
Synergies and trade-offs between ecosystem service supply, biodiversity, and habitat conservation status in Europe
Biol. Conserv.
An indicator framework for assessing ecosystem services in support of the EU Biodiversity Strategy to 2020
Ecosyst. Serv.
Embedding ecosystem services into the marine strategy framework directive: illustrated by eutrophication in the North Sea
Estuar. Coast. Shelf Sci.
Has the value of global marine and coastal ecosystem services changed?
Mar. Policy
Quantitative criteria for choosing targets and indicators for sustainable use of ecosystems
Ecol. Indic.
The quest for cryptic creatures: impacts of species-focused recreational diving on corals
Biol. Conserv.
A conceptual framework for assessing the ecosystem service of waste remediation: in the marine environment
Ecosyst. Serv.
Chapter 5: Identification of a practicable set of indicators for coastal and marine ecosystem services
Assessing costs and benefits of measures to achieve good environmental status in European regional seas: challenges, opportunities and lessons learnt
Front. Mar. Sci.
Linking biodiversity and ecosystem services: current uncertainties and the necessary next steps
Bioscience
Marine biodiversity, ecosystem functioning, and carbon cycles
Proc. Natl. Acad. Sci.
The marine strategy framework directive and the ecosystem-based approach −pitfalls and solutions
Mar. Pollut. Bull.
Tales from a thousand and one ways to integrate marine ecosystem components when assessing the environmental status
Front. Mar. Sci.
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