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Incorporating indirect ecosystem services into marine protected area planning and management

Incorporating indirect ecosystem services into marine protected area planning and management International Journal of Biodiversity Science, Ecosystem Services & Management Vol. 8, No. 3, September 2012, 273–285 a b a a Siân E. Rees *, Melanie C. Austen , Martin J. Attrill and Lynda D. Rodwell a b Marine Institute, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK; Plymouth Marine Laboratory, Plymouth, UK Marine Protected Areas (MPAs) are recognised as being the mechanism through which marine ecosystem services may be conserved to benefit human well-being. Planning and decision-making can be supported by the quantification and valuation of ecosystem services. To inform the development and management of MPAs a ‘service-orientated’ framework has been developed to use available data to spatially map and explore the pathways between ecosystem services, processes and the ecological functioning of benthic species for indirect ecosystem service provision within a case study area. The frame- work demonstrates that ecosystem service delivery is functionally interlinked and ecological function cannot be clearly mapped onto individual ecosystem services. The methodology developed here enables decision-makers to understand the links between benthic species, ecological function and indirect ecosystem services. There is currently no measure to quantify how much function is required to maintain human well-being. This lack of a measure, coupled with a large amount of uncer- tainty surrounding the links between ecosystem function and ecosystem service provision in marine systems, demonstrates that the inclusion of percentage targets for the conservation of broad-scale habitats in MPA planning and management should be considered within a precautionary approach to maintain the delivery of indirect ecosystem services. Keywords: biological traits analysis; ecosystem function; MPA; marine spatial planning; service-orientated framework Introduction biologically diverse oceans and seas’ (Department for Environment, Food and Rural Affairs 2002) the develop- Marine ecosystems provide a number of essential ecosys- ment of the Marine and Coastal Access Act (MCAA) (HM tem services, such as the provision of food and climate Government 2009), the Marine (Scotland) Act (2010) and regulation, which underpin life on earth. These ecosystem the forthcoming Northern Ireland Marine Bill (2012) pro- services form the constituent parts (e.g. food, shelter, clean vides the legal frameworks to develop Marine Plans water) that are essential to maintain human well-being (guided at a national level by the Marine Policy Statement (Millennium Ecosystem Assessment 2005; Beaumont et al. (HM Government 2011)). The development of Marine 2007; Austen et al. 2011). As such, these services are of Plans is led by the UK Marine Management Organisation value to humankind. (MMO). Two planning areas on the east coast of the Widespread and intensive human activity in the world’s United Kingdom are the first areas in England to be oceans and the subsequent loss of marine populations and selected for marine planning. It is the role of the MMO species are believed to be impairing the ability of marine to approve each plan for consultation and adoption. The ecosystems to provide the essential ecosystem services MCAA, the Marine (Scotland) Act (2010) and the forth- that contribute to human well-being (Chapin et al. 2000; coming Northern Ireland Marine Bill will also enable Hooper et al. 2005; Worm et al. 2006; Halpern et al. 2008). the designation of a new type of MPA called a marine Marine Protected Areas (MPAs), designated through a sys- conservation zone (MCZ). These commitments are under- tem of marine spatial planning, are recognised as being pinned by a requirement to adopt management measures to the mechanism through which marine ecosystem services enable the functioning of marine ecosystems to be main- may be conserved as ‘they are the only approach to marine tained (OSPAR Commission 2006; European Parliament resource management specifically designed to protect the and Council 2008; HM Government 2011). integrity of marine ecosystems and preserve intact portions Decision-making, especially where the natural environ- and examples of them’ (Sobel and Dahlgren 2004, p. 20). ment is concerned, is inherently exposed to high conflict In response to international and European drivers for potential (McShane et al. 2011; Minteer and Miller 2011) MPAs (European Community Council Directive 1992; thereby necessitating a methodology for capturing the com- OSPAR Convention 2002; Secretariat of the Convention plex context of ecosystem function and service provision on Biological Diversity 2004), the UK administrations are (Salafski et al. 2001). The development of descriptors tasked to substantially complete an ecologically coher- (Beaumont et al. 2007) to translate the complexity of ent network of MPAs by 2012 (HM Government 2011). marine ecosystem functions into marine ecosystem ser- To support the UK Government in meeting these inter- vices has broadened the inclusion of this range of values national and European commitments and to achieve the into decision-making for marine nature conservation. As a government’s aim of ‘clean, healthy, safe, productive and *Corresponding author. Email: sian.rees@plymouth.ac.uk ISSN 2151-3732 print/ISSN 2151-3740 online © 2012 Taylor & Francis http://dx.doi.org/10.1080/21513732.2012.680500 http://www.tandfonline.com 274 S.E. Rees et al. result, the consideration of economic, social and ecolog- In previous research relating to the marine environment ical values in decision-making (the ecosystem approach) BTA has been used to illustrate how ecosystems function through defining ecosystem services has therefore become in relation to the biological assemblages (Bremner et al. integral to marine conservation planning and policy in the 2006b; Frid et al. 2008) and in relation to time (Frid 2011). United Kingdom (OSPAR Commission 2006; European BTA has also proved useful as a tool to show how changes Parliament and Council 2008; HM Government 2009, in species composition caused by anthropogenic impacts 2011). affect ecosystem functioning (Tillin et al. 2006; Hewitt To inform the development of an ecosystem services et al. 2008). These studies have applied BTA to infer that framework and its application in marine conservation the ecological function of benthic species contributes to the planning and management, research is gathering pace on delivery of all ecosystem services. However, issues arise projects to spatially map and value ‘direct uses’ of the with this approach as marine managers, when working with marine environment, for example, recreation and fisheries stakeholders, may need to make trade-offs between differ- (Klein et al. 2008; Rees SE, Rodwell LD, et al. 2010). ent ecosystem services when decisions are made on the There has been less focus on ecological function partic- use of marine area (Kremen 2005). Managers will there- ularly for indirect ecosystem service provision which is fore need a more detailed understanding of how ecological defined as those benefits which are ‘derived from the envi- function is linked to these services and how they can be ronment without the intervention of man’ (Pearce and defined and valued at a local to regional scale (Loreau et al. Turner 1990; Beaumont et al. 2007). These services have 2001; Chan et al. 2006). not been measured directly in previous research for marine In this research a ‘service-orientated’ approach was planning as their delivery is considered to be functionally developed as this is most likely to translate across the interlinked by both biotic and abiotic processes (Hiscock science–policy interface (Kremen 2005; Raffaelli 2006). et al. 2006; Petchey and Gaston 2006; Bremner 2008). This The development of a framework for this research research therefore attempts to focus on the indirect regulat- follows the ‘ecosystem cascade’ theory developed by ing and supporting services in relation to biodiversity in a Haines-Young and Potschin (2007b) where the relation- case study area to inform marine planning. ship between biodiversity, ecosystem function and human There are variations on the definitions of indi- well-being is described in a simple linear framework. rect services (Constanza et al. 1997; De Groot et al. The complex concepts of ecosystem processes, functions 2002; Millennium Ecosystem Assessment 2005; Haines- and benefits act as prompts by which the complexities Young et al. 2007a; The Economics of Ecosystems and of ecosystem functioning, linked to services and human Biodiversity 2010). This research applies the definitions well-being, can be visualised to help understand a prob- of indirect ecosystem services for the marine environment lem (Haines-Young et al. 2007b). For a given case study following Beaumont et al. (2007) and Beaumont et al. area the services of interest are identified, followed by the (2006): identification of the processes and functions that affect the delivery of those services linked to the ecology of the gas and climate regulation (a regulating service): the case study marine area. Here, the framework was applied balance and maintenance of the chemical composi- to Lyme Bay in south-west England. To inform ongoing tion of the atmosphere and oceans by marine living debate regarding marine planning, conservation and the organisms; long-term delivery of ecosystem services the described research aims to (1) define the spatial area over which bioremediation of waste (a regulating service): the benthic species operate for the delivery of the indirect ser- removal of pollutants through storage, burial and vices of nutrient cycling, gas and climate regulation and recycling; and the bioremediation of waste in a case study area; (2) link nutrient cycling (a supporting service): the stor- the provision of services with current conservation policy; age, cycling and maintenance of nutrients by living and (3) make recommendations for the inclusion of indirect marine organisms. service provision in marine spatial planning policy. To define the importance (or value) of ecosystem functions in relation to ecosystem services previous research shows that the functional characteristics of species strongly influ- Materials and methods ences ecosystem processes (Hooper et al. 2005). Biological Case study area traits analysis (BTA) is a method which has been proposed to assess ecosystem function in marine benthic environ- Lyme Bay was chosen as it is a data-rich case study area. ments (Bremner et al. 2003, 2006a). BTA uses a series The offshore reef areas have been identified as a draft of behavioural (e.g. feeding), life history (e.g. age) and Special Area of Conservation under the European Union’s morphological characteristics (e.g. body size) of species to Habitats Directive (92/43/EEC) for the Annex 1 habitat define ecological function (Bremner et al. 2006b). The eco- criteria for reefs. Additionally, there is currently a 206 km logical function of a species is then used to infer an aspect statutory MPA within the bay. This closure was designated of ecosystem function (Lavorel and Garnier 2002; Bremner on 11 July 2008 by the UK Department for Environment, 2008). Food and Rural Affairs to protect the marine biodiversity International Journal of Biodiversity Science, Ecosystem Services & Management 275 Figure 1. The Lyme Bay case study area showing the 2008 closed area and substrate. Source of substrate data: Devon Biodiversity Records Centre. of the reefs from the impact of fishing with dredges and ongoing conservation planning activity both locally and other towed gear. regionally. The Lyme Bay study area is approximately 2460 km and is defined as the sea area which is enclosed by a line Data selection drawn between Portland Bill in Dorset and Start Point in Devon (Figure 1). This study focused on the benthic habi- Species distribution data (presence only) across 464 sur- tats which comprise of sublittoral rocky reefs (defined as vey sites (Figure 2) were extracted from three data sets, areas of rock and mixed ground in the northern section; made available by Devon Biodiversity Records Centre, mixed ground is defined as seabed consisting of com- Data Archive for Seabed Species and Habitats (www. binations of sand, gravel, pebbles, cobbles and boulders dassh.ac.uk) and the University of Plymouth: (Black 2007)), extending to soft sediment areas as the depth increases offshore. Lyme Bay has been identified as a sea search dive surveys (Wood 2007); ‘marine biodiversity hotspot’ (Hiscock and Breckels 2007). grab sample and drop video surveys undertaken by These are identified as areas of high species richness that Ambios Ltd on behalf of the Devon Wildlife Trust include rare and threatened species. The benthic habitats of (Ambios 2006); and Lyme Bay have been much studied (Rees SE, Attrill MJ, University of Plymouth drop video surveys (Stevens et al. 2010). To inform both statutory and non-statutory et al. 2007). marine spatial planning processes, extensive survey work to produce detailed biotope and substrate maps of Lyme These surveys were undertaken to quantify patterns of Bay was commissioned by the Devon Wildlife Trust in marine biodiversity at a scale relevant to marine spatial 2005 (Ambios 2006). These maps were further refined by planning within the case study area of Lyme Bay (Stevens Stevens et al. (2007). There is a large amount of available et al. 2007). These data are typical of the data available data relating to benthic assemblages. Any conclusions that to conservation planners and managers to inform their can be drawn from these data sets can be used to inform decision-making process. 276 S.E. Rees et al. Figure 2. Survey sites in Lyme Bay. A service-orientated framework and BTA Fourteen biological traits that relate directly to the ecosystem processes (Table 1) were chosen from a list The services of interest were identified, followed by the of 248 traits listed in the Biological Traits Information identification of the processes and functions that affect Catalogue (BIOTIC) (MarLIN 2006). the delivery of those services linked to the ecology of In order to comprehensively capture the function of Lyme Bay. The three ecosystem services selected for species in the case study area, multiple traits were selected study were nutrient cycling, gas and climate regulation and therefore several traits overlap within the same pro- and the bioremediation of waste. Nutrient cycling sup- cess (this is because not all records within BIOTIC ports the other two regulatory services but, in addition, are complete). For example, a species may be refer- these three services are highly interlinked in the marine enced in BIOTIC as being a ‘crawler’ under ‘movement environment through the functional roles performed by type’ (therefore exhibiting some bioturbator potential) but benthic species (Snelgrove 1998). Three ecosystem pro- not referenced as a ‘bioturbator’ under the category of cesses were selected which collectively and in combination ‘bioturbation’. The inclusion of multiple traits ensured that largely enable delivery of the three services, namely energy the role of each species would be included in the data fixation, energy transfer and the burial and enhancement analysis. If the species is recorded in BIOTIC as both a of microbial decomposition. Each of these processes can crawler and a bioturbator then it was only scored once be partially mapped onto the delivery of the three services within the process. Epifaunal and epibenthic species were (Table 1). only counted in the burial and enhancement of microbial A multi-trait approach was adopted that included as decomposition if they also expressed relevant traits under many traits as possible that are closely linked to these the movement, habit and bioturbation category. ecosystem processes. The aim of a multi-trait approach is The BIOTIC (MarLIN 2006, www.marlin.ac.uk/ to provide the most complete description of how the ecol- biotic) was used to determine the attribution of rele- ogy functions in the case study marine area (Bremner et al. vant biological traits for species found in the study area. 2006b; Bremner 2008). Species can be sorted into groups Of the total of 452 species identified from the survey data of effect traits that represent a functional role or that con- 383 species were successfully matched via the BIOTIC tribute to a process (Lavorel and Garnier 2002; Giller et al. database. 2004; Bremner et al. 2006a) (Table 1). International Journal of Biodiversity Science, Ecosystem Services & Management 277 Table 1. A service-orientated framework linking the provision of the ecosystem services of nutrient cycling, gas and climate regulation and the bioremediation of waste to functions that are influenced by the biological traits of benthic marine organisms. Ecosystem service Process Description Function References Trait category Trait Nutrient cycling Energy fixation The respiration of gases – Carbon fixation Bremner et al. Environmental Epifloral and the assimilation of – Nutrient cycling (2006a), Hiscock position Photoautotroph carbon and nutrients by – Respiration of gases et al. (2006) Feeding method primary producers to create biomass Gas and climate Energy transfer The respiration of gases, – Carbon assimilation Kristensen and Environmental Epifaunal/epibenthic regulation the excretion of organic – Trophic support and Blackburn position matter, the assimilation maintenance of marine (1987); Snelgrove Feeding method Active suspension of carbon and nutrients biomass (1997, 1998), feeder and the metabolising of – Consumption of Bremner et al. Passive suspension pollutants by secondary pollutants (2006a, 2006b) feeder producers operating at – Nutrient cycling Surface deposit the water column/ – Respiration of gases feeder surface interface – Resuspension of organic Interface feeder matter Bioremediation Enhancement of The role of secondary – Decomposition of organic Kristensen and Environmental Epifaunal/epibenthic of waste microbial producers in the burial of matter Blackburn (1987), position Infaunal decomposition organic matter and – Movement Snelgrove (1997, Movement Burrower supply of nutrients and – Consumption 1998), Petersen Crawler oxygen via bioturbation – Burial (sequestration) et al. (1998), Habit Tubicolous activities which enhance – Detoxification Pearson (2001), Burrow dweller the microbial – Cycling of organic Austen et al. Bioturbation Bioturbator decomposition process at materials and nutrients (2002), Bremner the surface/subsurface into and out of the et al. (2006a, interface sediment 2006b) Note: A definition of the traits can be accessed from BIOTIC (MarLIN 2006). 278 S.E. Rees et al. Data analysis data were joined spatially using the ESRI Arc GIS tool ‘Spatial Join’. The spatially joined data were re-exported to Each survey site was scored for the number of species Microsoft Excel to enable analysis of the data. To remove which demonstrate traits defined within the ecosystem sampling bias in the data (e.g. there are more species processes of energy fixation, energy transfer and the burial which display biological traits in the rock substrate as there and enhancement of microbial decomposition. Where a has been more sampling effort in this substrate type) the species demonstrated traits in more than one process (e.g. total for each key process within each substrate type was a species may be both a suspension feeder (energy trans- divided by the number of surveys undertaken, providing fer) and a burrower (enhancement of microbial decom- an average relative value for each key process within each position)) a score was given under each process. Where substrate type. a species demonstrated two or more traits within the same process (e.g. a species recorded within the BIOTIC database as both a burrower and a burrow dweller) the Results species would only be scored once. The scores were summed over each survey site providing a ‘process by site’ The BTA of species in Lyme Bay shows that the species matrix. To display the data spatially the ‘process by site’ which have traits that facilitate the key process of energy matrix was imported into GIS (ArcMap version 9.3.1). fixation are distinct from species which facilitate the Data were displayed using ‘graduated symbols’ where the key processes of energy transfer and the burial and size of the symbol indicated the relative score for each key enhancement of microbial decomposition within Lyme process at each site. The relative score (excluding sites Bay. Many species possess traits which facilitate both where 0 was recorded) was divided into five categories energy transfer and the burial and enhancement of micro- using Jenks optimisation method which classifies natural bial decomposition. breaks in the data by reducing variance within groups but The spatial results show (Figure 3) that the key pro- maximising variance between groups. cess of energy fixation occurs in the inshore waters of To enable an analysis of the three processes and the Lyme Bay. This analysis represents the epiflora and photo- relationship with substrate, the ‘process by site’ matrix autotrophs within Lyme Bay. Species which demonstrate Figure 3. The delivery of the process of energy fixation facilitated by benthic species in the Lyme Bay case study area. Note: Data are displayed as graduated symbols (Jenks optimisation) where the size of the symbol indicates the count for the process at a survey site. International Journal of Biodiversity Science, Ecosystem Services & Management 279 Figure 4. The delivery of the process of energy transfer facilitated by benthic species in the Lyme Bay case study area. Note: Data are displayed as graduated symbols (Jenks optimisation) where the size of the symbol indicates the count for the process at a survey site. traits that contribute towards the transfer of energy process Discussion can be seen within the protected (closed) area of Lyme Bay The ecosystem processes which can contribute to the deliv- (Figure 4) and on the rock and mixed substrates along the ery of the indirect ecosystem services of nutrient cycling, coast from Brixham to Start Point. They include species gas and climate regulation and the bioremediation of waste such as Alcyonium digitatum (Linnaeus) and Eunicella ver- are facilitated by the benthic flora and fauna across Lyme rucosa (Pallas). Benthic species which demonstrate the Bay. The main spatial differences are that the energy fix- traits that contribute towards the process of enhancement ation process is inevitably limited to the shallow waters of microbial decomposition were also found across all sites where light penetrates the water column enabling pri- in Lyme Bay (Figure 5). Relevant activities include the mary production in the benthos. Energy transfer and the burrowing of the bivalve mollusc Abra alba (Wood) and enhancement of microbial action are distributed broadly Arenicola marina (Linnaeus). across Lyme Bay with the former favouring the harder The substrates of mud, gravel and rock are the most substrates and the latter favouring the soft substrates. favourable for the energy fixation process as the sub- The results show that the MPA within Lyme Bay con- strate hosts species such as Zostera marina (Linnaeus), tains benthos which could potentially contribute to the Laminaria hyperborea (Gunnerus) and Lithothamnion delivery of the ecosystem services of gas and climate reg- corallioides (P & H Crouan). The mud and sand sub- ulation, the bioremediation of waste and nutrient cycling. strates are the least favourable for the presence of species However, the processes of energy fixation, energy transfer which demonstrate traits that facilitate energy transfer pro- and the burial and enhancement of microbial decompo- cesses in Lyme Bay (Figure 6). The soft substrates of mud sition are also delivered by benthic species across the and sand and mixed are more favourable for the enhance- substrate types throughout Lyme Bay. This raises numerous ment of microbial decomposition than the harder substrates points for discussion in relation to the practical application (Figure 6). of this methodology and how the ecological function for 280 S.E. Rees et al. Figure 5. The delivery of the process of burial and enhancement of microbial decomposition facilitated by benthic species in the Lyme Bay case study area. Note: Data are displayed as graduated symbols (Jenks optimisation) where the size of the symbol indicates the count for the process at a survey site. Figure 6. The relationship between substrate type and the delivery of the processes of energy fixation, energy transfer and the enhancement of microbial decomposition in the Lyme Bay case study area. Note: The standard error of the mean is shown for each process within each substrate type. International Journal of Biodiversity Science, Ecosystem Services & Management 281 indirect ecosystem services can be quantified and valued or the underpinning nutrient cycling is affected by human as required for conservation planning and management. uses of the benthic environment. Unless an entire trophic type was removed from the system it is unlikely that any local effects would be noticed. For example, a local extinc- How much function is there (value)? tion of filter feeders might cause increased turbidity. Unlike some direct use ecosystem services such as food provision The use of BTA in this context enabled exploration of how and recreation, which are experienced and managed across the indirect services can be spatially visualised and the local or regional scales, indirect services are broad, large potential for the benthic species to deliver these services. spatial-scale ecosystem services. This approach, however, does not enable the amount of In the near future, as marine spatial planning is imple- functioning to be quantified and therefore a measure of how mented, marine managers will be required to make deci- important these sites are in delivering the ecological func- sions and trade-offs between spatially different ecosystem tions and therefore a valuation of these ecosystem services services (Kremen 2005). In determining ‘how much func- is not possible to quantify. tion do we need?’ managers will require an understanding Previous research has focused on species richness of the potential contribution of all substrate types (and (species biodiversity) or the range of traits within bio- broad habitat types) to indirect service provision. They will logical assemblages (functional diversity) to indicate an also need to consider the impacts of human activities on the amount of functioning and therefore the delivery of all benthic environment and the sensitivity of some species to ecosystem services. However, no clearly defined relation- disturbance and how these in turn will affect service pro- ship between species diversity and ecosystem functioning vision. Methodological approaches that can measure the has been demonstrated (Chapin et al. 2000; Schwartz et al. delivery of ecosystem services in relation to indicators of 2000; Ieno et al. 2006; Somerfield et al. 2008). Although human well-being, for example, health via the develop- functional diversity is considered to be the most rele- ment of scenarios, may provide a more realistic picture vant indicator of the link between function and ecosystem of the delivery of these services and the impact on human services there is no standardised metric (Petchey and well-being (Bohensky et al. 2011). Gaston 2006; Somerfield et al. 2008). For example, a species may provide an ecological function that contributes to the delivery of all services or just one service (Petchey and Gaston 2006). There is also considered to be signifi- Other influences cant functional redundancy within the marine environment The delivery of indirect ecosystem services is not solely (Snelgrove 1997). In other words, areas that are func- linked to the ecological functions of benthic assemblages. tionally diverse may not provide more ecosystem func- Functioning is also affected by the physical and chemical tion. Furthermore, different scenarios of biodiversity loss properties of the system, for example, tidal currents and will affect the ecological function of benthos in differ- pH (Hiscock et al. 2006; Bremner 2008), as well as interac- ent ways (Solan et al. 2004). There is also a potential for tions between the pelagic and terrestrial systems. Analysis species substitutions to maintain ecological function as the of the whole system remains impossible because of a lack system changes over time (Frid 2011). This uncertainty of information on how these systems interact to provide makes it difficult to truly establish how subtle changes these broad ecosystem services (Petchey and Gaston 2006). in biodiversity will affect ecosystem services (Snelgrove Ecosystem functioning is also strongly linked to micro- 1998; Raffaelli 2006). bial groups present in the marine environment. For exam- It can be seen that the scientific foundations for valua- ple, in coral reef systems it has been found that the tion based on ecological function remain limited by a lack bioremediation of waste requires a diverse microbial com- of a measure for how much function a habitat provides. munity (Nystrom and Folke 2001). Exactly how the larger Recent calls from scientists in relation to the Convention macrobenthic organisms of this study impact upon micro- on Biological Diversity 2020 targets state that, although bial communities and hence impact upon microbially individual species have the capacity to provide a dispro- mediated ecosystem functions remains a research chal- portionate amount of service within a habitat area, there lenge (Petchey and Gaston 2006). is growing body of evidence that suggests that a measure of functional diversity would provide the best insurance for securing the delivery of ecosystem goods and services Can we plan for the long-term delivery of indirect (Perrings et al. 2010). Future developments in this field services? of valuation may focus on making a case for functionally Integrating ecosystem services into conservation planning diverse habitats in conservation planning and policy. and management remains a key challenge (De Groot et al. 2010). However, the concept of ecosystem services is an How much function do we need? example of where a framework developed by scientists has At present, on a local level in Lyme Bay or regionally, there translated well into policy, but the development of method- is no perception or evidence that maintenance of the global ologies to define and to value these ecosystem services has climate or the capacity of Lyme Bay to bioremediate waste raised numerous issues in its practical application. 282 S.E. Rees et al. Conservation planning in the marine environment Decision-makers must be aware that if they focus on valu- focuses on marine habitats and species and it has been ing the types of ecosystem services that are amenable to demonstrated in this research that the delivery of indi- economic value then it is possible that they may end up rect ecosystem services does not map neatly onto the only managing those economically valuable services at the presence of a particular species. Therefore, a consider- expense of the rest (Robinson 2011). ation of the conservation of broader habitat types, for In this study the use of BTA increased spatial awareness example, substrate as an insurance against the potential of where the links are between the ecological functions of loss of these ecosystem services, may provide the best benthic species and their potential to contribute towards option for ensuring the long-term delivery of indirect ser- the delivery of the ecosystem services of gas and climate vices. The UK Joint Nature Conservation Council and regulation, bioremediation of waste and nutrient cycling. Natural England (Ashworth and Stoker 2010) propose The fact that these services are functionally interlinked and that a network of MCZs should include percentage tar- cannot be directly mapped onto ecosystem service provi- gets for broad-scale habitats classified at the European sion indicates that if indirect services are to be included Nature Information System level 3 and percentage tar- in a cost–benefit or multi-criteria analysis for conservation gets for the inclusion of a select few species and habitats planning and management then managers must be aware identified for protection in existing conservation legisla- of the limitations of the available science to define and tion under the EU Habitats Directive, the UK Wildlife and quantify (or value) ecosystem function in relation to the Countryside Act (Biodiversity Action Plan species) and the delivery of ecosystem services; they must also be aware Oslo Paris Convention (OSPAR). This policy proposal is that the linear nature of the service-orientated framework an important step in recognising that all ecosystem ser- is a simplified model of ecosystem service delivery linked vices are not quantifiable and that conservation policy that to biodiversity and that there are ‘cascades’ and feedbacks focuses on biodiversity alone may result in areas which throughout the system (Haines-Young et al. 2007b). This are functionally important but not biodiverse being left out is important particularly if trade-offs are to be considered. of the planning process (Frid et al. 2008). The inclusion It should also be noted that the use of multiple traits to of percentage targets for broad-scale habitats in conserva- describe ecological function leads to a broad description of tion is an essential precautionary approach to maintain the ecological functioning (Bremner et al. 2006b) as the ‘real long-term delivery of indirect services. function’ is not represented. What is represented by the framework is an indication of the potential of biodiversity to provide the ecosystem services. Therefore, with such a Incorporating what we know into conservation broad field of variables within the marine environment the management and planning selection of specific traits that are sensitive to those impacts The use of BTA in the service-orientated framework relating to the management and conservation objectives for demonstrates that the conservation of the reef habitat in a marine site may help managers apply this tool to evalu- Lyme Bay secures a level of ecological function (and there- ate the effects of negative stressors (Elliott and Quintino fore value) to ensure the delivery of indirect ecosystem ser- 2007). vices of gas and climate regulation and the bioremediation of waste and nutrient cycling. The provision of those ser- Conclusion – including indirect ecosystem services into vices is not, however, exclusive to the MPA; they are MPA planning provided by species and habitats across the bay. This methodology provides an example of the prac- We recognise that this study develops only a partial assess- tical application of current science to available data for ment of ecosystem functioning in relation to indirect ser- the long-term delivery of indirect services. It demonstrates vice provision. Yet incorporating what is currently known that these indirect services can be visualised but they can- about the basic roles that marine species have in the not be valued. Valuations of ecosystems services remain delivery of ecosystem services, using available data, can central to the development of policy. The UK National inform the progress of management and policy relating Ecosystem Assessment, marine chapter, includes an eco- to the use and protection of the benthic natural resource. nomic analysis of the UK coastal margin and marine In this instance, the presence of species across Lyme habitats (Beaumont et al. 2010). Economic valuations Bay which contribute to the processes of energy transfer have also been provided for the required impact assess- and the enhancement of microbial decomposition provides ment to support the recommendations for a UK network a strong argument for the incorporation of the OSPAR of MCZs (Balanced Seas 2011; Irish Sea Conservation recommendations to include percentage targets for broad- Zones 2011; Leiberknecht et al. 2011; Net Gain 2011). scale habitats and to manage human activities within them. Such monetary valuations are important to maintain the In response to the lack of information on ecosystem func- importance of ecosystem services and human well-being tion, which species or habitats are critical for maintaining in policy. Indeed, when applied spatially in a planning con- function and the delivery ecosystem services in the marine text they can show the relative economic importance of environment, there is a need to include ‘precaution’ and an activity. However, it is in its practical application for ‘uncertainty’ into the planning process (Balvanera et al. planning and management that caution must be exercised. 2006; Bulling et al. 2010; Foley et al. 2010). A ‘protect International Journal of Biodiversity Science, Ecosystem Services & Management 283 a bit of everything’ approach is largely precautionary and Beaumont N, Hattam C, Mangi S, Moran D, Soest Dv, Jones L, Toberman M. 2010. 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Incorporating indirect ecosystem services into marine protected area planning and management

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Abstract

International Journal of Biodiversity Science, Ecosystem Services & Management Vol. 8, No. 3, September 2012, 273–285 a b a a Siân E. Rees *, Melanie C. Austen , Martin J. Attrill and Lynda D. Rodwell a b Marine Institute, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK; Plymouth Marine Laboratory, Plymouth, UK Marine Protected Areas (MPAs) are recognised as being the mechanism through which marine ecosystem services may be conserved to benefit human well-being. Planning and decision-making can be supported by the quantification and valuation of ecosystem services. To inform the development and management of MPAs a ‘service-orientated’ framework has been developed to use available data to spatially map and explore the pathways between ecosystem services, processes and the ecological functioning of benthic species for indirect ecosystem service provision within a case study area. The frame- work demonstrates that ecosystem service delivery is functionally interlinked and ecological function cannot be clearly mapped onto individual ecosystem services. The methodology developed here enables decision-makers to understand the links between benthic species, ecological function and indirect ecosystem services. There is currently no measure to quantify how much function is required to maintain human well-being. This lack of a measure, coupled with a large amount of uncer- tainty surrounding the links between ecosystem function and ecosystem service provision in marine systems, demonstrates that the inclusion of percentage targets for the conservation of broad-scale habitats in MPA planning and management should be considered within a precautionary approach to maintain the delivery of indirect ecosystem services. Keywords: biological traits analysis; ecosystem function; MPA; marine spatial planning; service-orientated framework Introduction biologically diverse oceans and seas’ (Department for Environment, Food and Rural Affairs 2002) the develop- Marine ecosystems provide a number of essential ecosys- ment of the Marine and Coastal Access Act (MCAA) (HM tem services, such as the provision of food and climate Government 2009), the Marine (Scotland) Act (2010) and regulation, which underpin life on earth. These ecosystem the forthcoming Northern Ireland Marine Bill (2012) pro- services form the constituent parts (e.g. food, shelter, clean vides the legal frameworks to develop Marine Plans water) that are essential to maintain human well-being (guided at a national level by the Marine Policy Statement (Millennium Ecosystem Assessment 2005; Beaumont et al. (HM Government 2011)). The development of Marine 2007; Austen et al. 2011). As such, these services are of Plans is led by the UK Marine Management Organisation value to humankind. (MMO). Two planning areas on the east coast of the Widespread and intensive human activity in the world’s United Kingdom are the first areas in England to be oceans and the subsequent loss of marine populations and selected for marine planning. It is the role of the MMO species are believed to be impairing the ability of marine to approve each plan for consultation and adoption. The ecosystems to provide the essential ecosystem services MCAA, the Marine (Scotland) Act (2010) and the forth- that contribute to human well-being (Chapin et al. 2000; coming Northern Ireland Marine Bill will also enable Hooper et al. 2005; Worm et al. 2006; Halpern et al. 2008). the designation of a new type of MPA called a marine Marine Protected Areas (MPAs), designated through a sys- conservation zone (MCZ). These commitments are under- tem of marine spatial planning, are recognised as being pinned by a requirement to adopt management measures to the mechanism through which marine ecosystem services enable the functioning of marine ecosystems to be main- may be conserved as ‘they are the only approach to marine tained (OSPAR Commission 2006; European Parliament resource management specifically designed to protect the and Council 2008; HM Government 2011). integrity of marine ecosystems and preserve intact portions Decision-making, especially where the natural environ- and examples of them’ (Sobel and Dahlgren 2004, p. 20). ment is concerned, is inherently exposed to high conflict In response to international and European drivers for potential (McShane et al. 2011; Minteer and Miller 2011) MPAs (European Community Council Directive 1992; thereby necessitating a methodology for capturing the com- OSPAR Convention 2002; Secretariat of the Convention plex context of ecosystem function and service provision on Biological Diversity 2004), the UK administrations are (Salafski et al. 2001). The development of descriptors tasked to substantially complete an ecologically coher- (Beaumont et al. 2007) to translate the complexity of ent network of MPAs by 2012 (HM Government 2011). marine ecosystem functions into marine ecosystem ser- To support the UK Government in meeting these inter- vices has broadened the inclusion of this range of values national and European commitments and to achieve the into decision-making for marine nature conservation. As a government’s aim of ‘clean, healthy, safe, productive and *Corresponding author. Email: sian.rees@plymouth.ac.uk ISSN 2151-3732 print/ISSN 2151-3740 online © 2012 Taylor & Francis http://dx.doi.org/10.1080/21513732.2012.680500 http://www.tandfonline.com 274 S.E. Rees et al. result, the consideration of economic, social and ecolog- In previous research relating to the marine environment ical values in decision-making (the ecosystem approach) BTA has been used to illustrate how ecosystems function through defining ecosystem services has therefore become in relation to the biological assemblages (Bremner et al. integral to marine conservation planning and policy in the 2006b; Frid et al. 2008) and in relation to time (Frid 2011). United Kingdom (OSPAR Commission 2006; European BTA has also proved useful as a tool to show how changes Parliament and Council 2008; HM Government 2009, in species composition caused by anthropogenic impacts 2011). affect ecosystem functioning (Tillin et al. 2006; Hewitt To inform the development of an ecosystem services et al. 2008). These studies have applied BTA to infer that framework and its application in marine conservation the ecological function of benthic species contributes to the planning and management, research is gathering pace on delivery of all ecosystem services. However, issues arise projects to spatially map and value ‘direct uses’ of the with this approach as marine managers, when working with marine environment, for example, recreation and fisheries stakeholders, may need to make trade-offs between differ- (Klein et al. 2008; Rees SE, Rodwell LD, et al. 2010). ent ecosystem services when decisions are made on the There has been less focus on ecological function partic- use of marine area (Kremen 2005). Managers will there- ularly for indirect ecosystem service provision which is fore need a more detailed understanding of how ecological defined as those benefits which are ‘derived from the envi- function is linked to these services and how they can be ronment without the intervention of man’ (Pearce and defined and valued at a local to regional scale (Loreau et al. Turner 1990; Beaumont et al. 2007). These services have 2001; Chan et al. 2006). not been measured directly in previous research for marine In this research a ‘service-orientated’ approach was planning as their delivery is considered to be functionally developed as this is most likely to translate across the interlinked by both biotic and abiotic processes (Hiscock science–policy interface (Kremen 2005; Raffaelli 2006). et al. 2006; Petchey and Gaston 2006; Bremner 2008). This The development of a framework for this research research therefore attempts to focus on the indirect regulat- follows the ‘ecosystem cascade’ theory developed by ing and supporting services in relation to biodiversity in a Haines-Young and Potschin (2007b) where the relation- case study area to inform marine planning. ship between biodiversity, ecosystem function and human There are variations on the definitions of indi- well-being is described in a simple linear framework. rect services (Constanza et al. 1997; De Groot et al. The complex concepts of ecosystem processes, functions 2002; Millennium Ecosystem Assessment 2005; Haines- and benefits act as prompts by which the complexities Young et al. 2007a; The Economics of Ecosystems and of ecosystem functioning, linked to services and human Biodiversity 2010). This research applies the definitions well-being, can be visualised to help understand a prob- of indirect ecosystem services for the marine environment lem (Haines-Young et al. 2007b). For a given case study following Beaumont et al. (2007) and Beaumont et al. area the services of interest are identified, followed by the (2006): identification of the processes and functions that affect the delivery of those services linked to the ecology of the gas and climate regulation (a regulating service): the case study marine area. Here, the framework was applied balance and maintenance of the chemical composi- to Lyme Bay in south-west England. To inform ongoing tion of the atmosphere and oceans by marine living debate regarding marine planning, conservation and the organisms; long-term delivery of ecosystem services the described research aims to (1) define the spatial area over which bioremediation of waste (a regulating service): the benthic species operate for the delivery of the indirect ser- removal of pollutants through storage, burial and vices of nutrient cycling, gas and climate regulation and recycling; and the bioremediation of waste in a case study area; (2) link nutrient cycling (a supporting service): the stor- the provision of services with current conservation policy; age, cycling and maintenance of nutrients by living and (3) make recommendations for the inclusion of indirect marine organisms. service provision in marine spatial planning policy. To define the importance (or value) of ecosystem functions in relation to ecosystem services previous research shows that the functional characteristics of species strongly influ- Materials and methods ences ecosystem processes (Hooper et al. 2005). Biological Case study area traits analysis (BTA) is a method which has been proposed to assess ecosystem function in marine benthic environ- Lyme Bay was chosen as it is a data-rich case study area. ments (Bremner et al. 2003, 2006a). BTA uses a series The offshore reef areas have been identified as a draft of behavioural (e.g. feeding), life history (e.g. age) and Special Area of Conservation under the European Union’s morphological characteristics (e.g. body size) of species to Habitats Directive (92/43/EEC) for the Annex 1 habitat define ecological function (Bremner et al. 2006b). The eco- criteria for reefs. Additionally, there is currently a 206 km logical function of a species is then used to infer an aspect statutory MPA within the bay. This closure was designated of ecosystem function (Lavorel and Garnier 2002; Bremner on 11 July 2008 by the UK Department for Environment, 2008). Food and Rural Affairs to protect the marine biodiversity International Journal of Biodiversity Science, Ecosystem Services & Management 275 Figure 1. The Lyme Bay case study area showing the 2008 closed area and substrate. Source of substrate data: Devon Biodiversity Records Centre. of the reefs from the impact of fishing with dredges and ongoing conservation planning activity both locally and other towed gear. regionally. The Lyme Bay study area is approximately 2460 km and is defined as the sea area which is enclosed by a line Data selection drawn between Portland Bill in Dorset and Start Point in Devon (Figure 1). This study focused on the benthic habi- Species distribution data (presence only) across 464 sur- tats which comprise of sublittoral rocky reefs (defined as vey sites (Figure 2) were extracted from three data sets, areas of rock and mixed ground in the northern section; made available by Devon Biodiversity Records Centre, mixed ground is defined as seabed consisting of com- Data Archive for Seabed Species and Habitats (www. binations of sand, gravel, pebbles, cobbles and boulders dassh.ac.uk) and the University of Plymouth: (Black 2007)), extending to soft sediment areas as the depth increases offshore. Lyme Bay has been identified as a sea search dive surveys (Wood 2007); ‘marine biodiversity hotspot’ (Hiscock and Breckels 2007). grab sample and drop video surveys undertaken by These are identified as areas of high species richness that Ambios Ltd on behalf of the Devon Wildlife Trust include rare and threatened species. The benthic habitats of (Ambios 2006); and Lyme Bay have been much studied (Rees SE, Attrill MJ, University of Plymouth drop video surveys (Stevens et al. 2010). To inform both statutory and non-statutory et al. 2007). marine spatial planning processes, extensive survey work to produce detailed biotope and substrate maps of Lyme These surveys were undertaken to quantify patterns of Bay was commissioned by the Devon Wildlife Trust in marine biodiversity at a scale relevant to marine spatial 2005 (Ambios 2006). These maps were further refined by planning within the case study area of Lyme Bay (Stevens Stevens et al. (2007). There is a large amount of available et al. 2007). These data are typical of the data available data relating to benthic assemblages. Any conclusions that to conservation planners and managers to inform their can be drawn from these data sets can be used to inform decision-making process. 276 S.E. Rees et al. Figure 2. Survey sites in Lyme Bay. A service-orientated framework and BTA Fourteen biological traits that relate directly to the ecosystem processes (Table 1) were chosen from a list The services of interest were identified, followed by the of 248 traits listed in the Biological Traits Information identification of the processes and functions that affect Catalogue (BIOTIC) (MarLIN 2006). the delivery of those services linked to the ecology of In order to comprehensively capture the function of Lyme Bay. The three ecosystem services selected for species in the case study area, multiple traits were selected study were nutrient cycling, gas and climate regulation and therefore several traits overlap within the same pro- and the bioremediation of waste. Nutrient cycling sup- cess (this is because not all records within BIOTIC ports the other two regulatory services but, in addition, are complete). For example, a species may be refer- these three services are highly interlinked in the marine enced in BIOTIC as being a ‘crawler’ under ‘movement environment through the functional roles performed by type’ (therefore exhibiting some bioturbator potential) but benthic species (Snelgrove 1998). Three ecosystem pro- not referenced as a ‘bioturbator’ under the category of cesses were selected which collectively and in combination ‘bioturbation’. The inclusion of multiple traits ensured that largely enable delivery of the three services, namely energy the role of each species would be included in the data fixation, energy transfer and the burial and enhancement analysis. If the species is recorded in BIOTIC as both a of microbial decomposition. Each of these processes can crawler and a bioturbator then it was only scored once be partially mapped onto the delivery of the three services within the process. Epifaunal and epibenthic species were (Table 1). only counted in the burial and enhancement of microbial A multi-trait approach was adopted that included as decomposition if they also expressed relevant traits under many traits as possible that are closely linked to these the movement, habit and bioturbation category. ecosystem processes. The aim of a multi-trait approach is The BIOTIC (MarLIN 2006, www.marlin.ac.uk/ to provide the most complete description of how the ecol- biotic) was used to determine the attribution of rele- ogy functions in the case study marine area (Bremner et al. vant biological traits for species found in the study area. 2006b; Bremner 2008). Species can be sorted into groups Of the total of 452 species identified from the survey data of effect traits that represent a functional role or that con- 383 species were successfully matched via the BIOTIC tribute to a process (Lavorel and Garnier 2002; Giller et al. database. 2004; Bremner et al. 2006a) (Table 1). International Journal of Biodiversity Science, Ecosystem Services & Management 277 Table 1. A service-orientated framework linking the provision of the ecosystem services of nutrient cycling, gas and climate regulation and the bioremediation of waste to functions that are influenced by the biological traits of benthic marine organisms. Ecosystem service Process Description Function References Trait category Trait Nutrient cycling Energy fixation The respiration of gases – Carbon fixation Bremner et al. Environmental Epifloral and the assimilation of – Nutrient cycling (2006a), Hiscock position Photoautotroph carbon and nutrients by – Respiration of gases et al. (2006) Feeding method primary producers to create biomass Gas and climate Energy transfer The respiration of gases, – Carbon assimilation Kristensen and Environmental Epifaunal/epibenthic regulation the excretion of organic – Trophic support and Blackburn position matter, the assimilation maintenance of marine (1987); Snelgrove Feeding method Active suspension of carbon and nutrients biomass (1997, 1998), feeder and the metabolising of – Consumption of Bremner et al. Passive suspension pollutants by secondary pollutants (2006a, 2006b) feeder producers operating at – Nutrient cycling Surface deposit the water column/ – Respiration of gases feeder surface interface – Resuspension of organic Interface feeder matter Bioremediation Enhancement of The role of secondary – Decomposition of organic Kristensen and Environmental Epifaunal/epibenthic of waste microbial producers in the burial of matter Blackburn (1987), position Infaunal decomposition organic matter and – Movement Snelgrove (1997, Movement Burrower supply of nutrients and – Consumption 1998), Petersen Crawler oxygen via bioturbation – Burial (sequestration) et al. (1998), Habit Tubicolous activities which enhance – Detoxification Pearson (2001), Burrow dweller the microbial – Cycling of organic Austen et al. Bioturbation Bioturbator decomposition process at materials and nutrients (2002), Bremner the surface/subsurface into and out of the et al. (2006a, interface sediment 2006b) Note: A definition of the traits can be accessed from BIOTIC (MarLIN 2006). 278 S.E. Rees et al. Data analysis data were joined spatially using the ESRI Arc GIS tool ‘Spatial Join’. The spatially joined data were re-exported to Each survey site was scored for the number of species Microsoft Excel to enable analysis of the data. To remove which demonstrate traits defined within the ecosystem sampling bias in the data (e.g. there are more species processes of energy fixation, energy transfer and the burial which display biological traits in the rock substrate as there and enhancement of microbial decomposition. Where a has been more sampling effort in this substrate type) the species demonstrated traits in more than one process (e.g. total for each key process within each substrate type was a species may be both a suspension feeder (energy trans- divided by the number of surveys undertaken, providing fer) and a burrower (enhancement of microbial decom- an average relative value for each key process within each position)) a score was given under each process. Where substrate type. a species demonstrated two or more traits within the same process (e.g. a species recorded within the BIOTIC database as both a burrower and a burrow dweller) the Results species would only be scored once. The scores were summed over each survey site providing a ‘process by site’ The BTA of species in Lyme Bay shows that the species matrix. To display the data spatially the ‘process by site’ which have traits that facilitate the key process of energy matrix was imported into GIS (ArcMap version 9.3.1). fixation are distinct from species which facilitate the Data were displayed using ‘graduated symbols’ where the key processes of energy transfer and the burial and size of the symbol indicated the relative score for each key enhancement of microbial decomposition within Lyme process at each site. The relative score (excluding sites Bay. Many species possess traits which facilitate both where 0 was recorded) was divided into five categories energy transfer and the burial and enhancement of micro- using Jenks optimisation method which classifies natural bial decomposition. breaks in the data by reducing variance within groups but The spatial results show (Figure 3) that the key pro- maximising variance between groups. cess of energy fixation occurs in the inshore waters of To enable an analysis of the three processes and the Lyme Bay. This analysis represents the epiflora and photo- relationship with substrate, the ‘process by site’ matrix autotrophs within Lyme Bay. Species which demonstrate Figure 3. The delivery of the process of energy fixation facilitated by benthic species in the Lyme Bay case study area. Note: Data are displayed as graduated symbols (Jenks optimisation) where the size of the symbol indicates the count for the process at a survey site. International Journal of Biodiversity Science, Ecosystem Services & Management 279 Figure 4. The delivery of the process of energy transfer facilitated by benthic species in the Lyme Bay case study area. Note: Data are displayed as graduated symbols (Jenks optimisation) where the size of the symbol indicates the count for the process at a survey site. traits that contribute towards the transfer of energy process Discussion can be seen within the protected (closed) area of Lyme Bay The ecosystem processes which can contribute to the deliv- (Figure 4) and on the rock and mixed substrates along the ery of the indirect ecosystem services of nutrient cycling, coast from Brixham to Start Point. They include species gas and climate regulation and the bioremediation of waste such as Alcyonium digitatum (Linnaeus) and Eunicella ver- are facilitated by the benthic flora and fauna across Lyme rucosa (Pallas). Benthic species which demonstrate the Bay. The main spatial differences are that the energy fix- traits that contribute towards the process of enhancement ation process is inevitably limited to the shallow waters of microbial decomposition were also found across all sites where light penetrates the water column enabling pri- in Lyme Bay (Figure 5). Relevant activities include the mary production in the benthos. Energy transfer and the burrowing of the bivalve mollusc Abra alba (Wood) and enhancement of microbial action are distributed broadly Arenicola marina (Linnaeus). across Lyme Bay with the former favouring the harder The substrates of mud, gravel and rock are the most substrates and the latter favouring the soft substrates. favourable for the energy fixation process as the sub- The results show that the MPA within Lyme Bay con- strate hosts species such as Zostera marina (Linnaeus), tains benthos which could potentially contribute to the Laminaria hyperborea (Gunnerus) and Lithothamnion delivery of the ecosystem services of gas and climate reg- corallioides (P & H Crouan). The mud and sand sub- ulation, the bioremediation of waste and nutrient cycling. strates are the least favourable for the presence of species However, the processes of energy fixation, energy transfer which demonstrate traits that facilitate energy transfer pro- and the burial and enhancement of microbial decompo- cesses in Lyme Bay (Figure 6). The soft substrates of mud sition are also delivered by benthic species across the and sand and mixed are more favourable for the enhance- substrate types throughout Lyme Bay. This raises numerous ment of microbial decomposition than the harder substrates points for discussion in relation to the practical application (Figure 6). of this methodology and how the ecological function for 280 S.E. Rees et al. Figure 5. The delivery of the process of burial and enhancement of microbial decomposition facilitated by benthic species in the Lyme Bay case study area. Note: Data are displayed as graduated symbols (Jenks optimisation) where the size of the symbol indicates the count for the process at a survey site. Figure 6. The relationship between substrate type and the delivery of the processes of energy fixation, energy transfer and the enhancement of microbial decomposition in the Lyme Bay case study area. Note: The standard error of the mean is shown for each process within each substrate type. International Journal of Biodiversity Science, Ecosystem Services & Management 281 indirect ecosystem services can be quantified and valued or the underpinning nutrient cycling is affected by human as required for conservation planning and management. uses of the benthic environment. Unless an entire trophic type was removed from the system it is unlikely that any local effects would be noticed. For example, a local extinc- How much function is there (value)? tion of filter feeders might cause increased turbidity. Unlike some direct use ecosystem services such as food provision The use of BTA in this context enabled exploration of how and recreation, which are experienced and managed across the indirect services can be spatially visualised and the local or regional scales, indirect services are broad, large potential for the benthic species to deliver these services. spatial-scale ecosystem services. This approach, however, does not enable the amount of In the near future, as marine spatial planning is imple- functioning to be quantified and therefore a measure of how mented, marine managers will be required to make deci- important these sites are in delivering the ecological func- sions and trade-offs between spatially different ecosystem tions and therefore a valuation of these ecosystem services services (Kremen 2005). In determining ‘how much func- is not possible to quantify. tion do we need?’ managers will require an understanding Previous research has focused on species richness of the potential contribution of all substrate types (and (species biodiversity) or the range of traits within bio- broad habitat types) to indirect service provision. They will logical assemblages (functional diversity) to indicate an also need to consider the impacts of human activities on the amount of functioning and therefore the delivery of all benthic environment and the sensitivity of some species to ecosystem services. However, no clearly defined relation- disturbance and how these in turn will affect service pro- ship between species diversity and ecosystem functioning vision. Methodological approaches that can measure the has been demonstrated (Chapin et al. 2000; Schwartz et al. delivery of ecosystem services in relation to indicators of 2000; Ieno et al. 2006; Somerfield et al. 2008). Although human well-being, for example, health via the develop- functional diversity is considered to be the most rele- ment of scenarios, may provide a more realistic picture vant indicator of the link between function and ecosystem of the delivery of these services and the impact on human services there is no standardised metric (Petchey and well-being (Bohensky et al. 2011). Gaston 2006; Somerfield et al. 2008). For example, a species may provide an ecological function that contributes to the delivery of all services or just one service (Petchey and Gaston 2006). There is also considered to be signifi- Other influences cant functional redundancy within the marine environment The delivery of indirect ecosystem services is not solely (Snelgrove 1997). In other words, areas that are func- linked to the ecological functions of benthic assemblages. tionally diverse may not provide more ecosystem func- Functioning is also affected by the physical and chemical tion. Furthermore, different scenarios of biodiversity loss properties of the system, for example, tidal currents and will affect the ecological function of benthos in differ- pH (Hiscock et al. 2006; Bremner 2008), as well as interac- ent ways (Solan et al. 2004). There is also a potential for tions between the pelagic and terrestrial systems. Analysis species substitutions to maintain ecological function as the of the whole system remains impossible because of a lack system changes over time (Frid 2011). This uncertainty of information on how these systems interact to provide makes it difficult to truly establish how subtle changes these broad ecosystem services (Petchey and Gaston 2006). in biodiversity will affect ecosystem services (Snelgrove Ecosystem functioning is also strongly linked to micro- 1998; Raffaelli 2006). bial groups present in the marine environment. For exam- It can be seen that the scientific foundations for valua- ple, in coral reef systems it has been found that the tion based on ecological function remain limited by a lack bioremediation of waste requires a diverse microbial com- of a measure for how much function a habitat provides. munity (Nystrom and Folke 2001). Exactly how the larger Recent calls from scientists in relation to the Convention macrobenthic organisms of this study impact upon micro- on Biological Diversity 2020 targets state that, although bial communities and hence impact upon microbially individual species have the capacity to provide a dispro- mediated ecosystem functions remains a research chal- portionate amount of service within a habitat area, there lenge (Petchey and Gaston 2006). is growing body of evidence that suggests that a measure of functional diversity would provide the best insurance for securing the delivery of ecosystem goods and services Can we plan for the long-term delivery of indirect (Perrings et al. 2010). Future developments in this field services? of valuation may focus on making a case for functionally Integrating ecosystem services into conservation planning diverse habitats in conservation planning and policy. and management remains a key challenge (De Groot et al. 2010). However, the concept of ecosystem services is an How much function do we need? example of where a framework developed by scientists has At present, on a local level in Lyme Bay or regionally, there translated well into policy, but the development of method- is no perception or evidence that maintenance of the global ologies to define and to value these ecosystem services has climate or the capacity of Lyme Bay to bioremediate waste raised numerous issues in its practical application. 282 S.E. Rees et al. Conservation planning in the marine environment Decision-makers must be aware that if they focus on valu- focuses on marine habitats and species and it has been ing the types of ecosystem services that are amenable to demonstrated in this research that the delivery of indi- economic value then it is possible that they may end up rect ecosystem services does not map neatly onto the only managing those economically valuable services at the presence of a particular species. Therefore, a consider- expense of the rest (Robinson 2011). ation of the conservation of broader habitat types, for In this study the use of BTA increased spatial awareness example, substrate as an insurance against the potential of where the links are between the ecological functions of loss of these ecosystem services, may provide the best benthic species and their potential to contribute towards option for ensuring the long-term delivery of indirect ser- the delivery of the ecosystem services of gas and climate vices. The UK Joint Nature Conservation Council and regulation, bioremediation of waste and nutrient cycling. Natural England (Ashworth and Stoker 2010) propose The fact that these services are functionally interlinked and that a network of MCZs should include percentage tar- cannot be directly mapped onto ecosystem service provi- gets for broad-scale habitats classified at the European sion indicates that if indirect services are to be included Nature Information System level 3 and percentage tar- in a cost–benefit or multi-criteria analysis for conservation gets for the inclusion of a select few species and habitats planning and management then managers must be aware identified for protection in existing conservation legisla- of the limitations of the available science to define and tion under the EU Habitats Directive, the UK Wildlife and quantify (or value) ecosystem function in relation to the Countryside Act (Biodiversity Action Plan species) and the delivery of ecosystem services; they must also be aware Oslo Paris Convention (OSPAR). This policy proposal is that the linear nature of the service-orientated framework an important step in recognising that all ecosystem ser- is a simplified model of ecosystem service delivery linked vices are not quantifiable and that conservation policy that to biodiversity and that there are ‘cascades’ and feedbacks focuses on biodiversity alone may result in areas which throughout the system (Haines-Young et al. 2007b). This are functionally important but not biodiverse being left out is important particularly if trade-offs are to be considered. of the planning process (Frid et al. 2008). The inclusion It should also be noted that the use of multiple traits to of percentage targets for broad-scale habitats in conserva- describe ecological function leads to a broad description of tion is an essential precautionary approach to maintain the ecological functioning (Bremner et al. 2006b) as the ‘real long-term delivery of indirect services. function’ is not represented. What is represented by the framework is an indication of the potential of biodiversity to provide the ecosystem services. Therefore, with such a Incorporating what we know into conservation broad field of variables within the marine environment the management and planning selection of specific traits that are sensitive to those impacts The use of BTA in the service-orientated framework relating to the management and conservation objectives for demonstrates that the conservation of the reef habitat in a marine site may help managers apply this tool to evalu- Lyme Bay secures a level of ecological function (and there- ate the effects of negative stressors (Elliott and Quintino fore value) to ensure the delivery of indirect ecosystem ser- 2007). vices of gas and climate regulation and the bioremediation of waste and nutrient cycling. The provision of those ser- Conclusion – including indirect ecosystem services into vices is not, however, exclusive to the MPA; they are MPA planning provided by species and habitats across the bay. This methodology provides an example of the prac- We recognise that this study develops only a partial assess- tical application of current science to available data for ment of ecosystem functioning in relation to indirect ser- the long-term delivery of indirect services. It demonstrates vice provision. Yet incorporating what is currently known that these indirect services can be visualised but they can- about the basic roles that marine species have in the not be valued. Valuations of ecosystems services remain delivery of ecosystem services, using available data, can central to the development of policy. The UK National inform the progress of management and policy relating Ecosystem Assessment, marine chapter, includes an eco- to the use and protection of the benthic natural resource. nomic analysis of the UK coastal margin and marine In this instance, the presence of species across Lyme habitats (Beaumont et al. 2010). Economic valuations Bay which contribute to the processes of energy transfer have also been provided for the required impact assess- and the enhancement of microbial decomposition provides ment to support the recommendations for a UK network a strong argument for the incorporation of the OSPAR of MCZs (Balanced Seas 2011; Irish Sea Conservation recommendations to include percentage targets for broad- Zones 2011; Leiberknecht et al. 2011; Net Gain 2011). scale habitats and to manage human activities within them. Such monetary valuations are important to maintain the In response to the lack of information on ecosystem func- importance of ecosystem services and human well-being tion, which species or habitats are critical for maintaining in policy. Indeed, when applied spatially in a planning con- function and the delivery ecosystem services in the marine text they can show the relative economic importance of environment, there is a need to include ‘precaution’ and an activity. However, it is in its practical application for ‘uncertainty’ into the planning process (Balvanera et al. planning and management that caution must be exercised. 2006; Bulling et al. 2010; Foley et al. 2010). A ‘protect International Journal of Biodiversity Science, Ecosystem Services & Management 283 a bit of everything’ approach is largely precautionary and Beaumont N, Hattam C, Mangi S, Moran D, Soest Dv, Jones L, Toberman M. 2010. National ecosystem assessment: should remain open to the principles of adaptive manage- economic analysis coastal margin and marine habitats. Final ment (Salafski et al. 2001) as our understanding of the links Report. UK NEA Economic Analysis Reports. p. 96. [cited between ecology, divers for change, ecosystem function 2012 Apr 16]. Available from: http://uknea.unep-wcmc.org/ and the delivery of ecosystem services improves. Resources/tabid/82/Default.aspx In terms of the development of research from the Beaumont N, Townsend M, Mangi S, Austen MC. 2006. Marine biodiversity an economic valuation. Building the evidence ‘ecosystem services community’ to support marine con- base for a Marine Bill. London (UK): DEFRA. A DEFRA servation planning and policy this research has shown that Report. there is a need to further refine the BTA methodology Beaumont NJ, Austen MC, Atkins JP, Burdon D, Degraer S, so that ecological function can be quantified at a local to Dentinho TP, Derous S, Holm P, Horton T, Ierland Ev, regional scale. In lieu of perfect ecosystem function mod- et al. 2007. Identification, definition and quantification of goods and services provided by marine biodiversity: impli- els for the marine environment, research could support the cations for the ecosystem approach. Mar Pollut Bull. 54(3): development of a ‘shortlist’ of biological indicator traits 253–265. that can provide a measure of the negative effect of environ- Black G. 2007. Lyme Bay Pink Sea Fan Survey 2006–2007. A mental stressors. These indicators would be useful for man- report by Devon Biodiversity Records Centre. Devon (UK): agers to monitor the impact of activities in a marine area. DBRC. p. 33. Bohensky E, Butler JRA, Costanza R, Bohnet I, Delisle A, Fabricius K, Gooch M, Kubiszewski I, Lukacs G, Pert P, et al. 2011. Future makers or future takers? A scenario analysis of Acknowledgements climate change and the Great Barrier Reef. Global Environ All substrate maps have been derived from data provided by Change. 21(3):876–893. Devon Biodiversity Records Centre, for which copyright belongs Bremner J. 2008. Species’ traits and ecological functioning in to a variety of organisations including UK Hydrographic Office marine conservation and management. J Exp Mar Biol Ecol. and Devon Wildlife Trust and for which permission for use in 366(1–2):37–47. this instance has been granted. No further copies may be made. Bremner J, Rogers SI, Frid CLJ. 2003. Assessing functional This research has been enabled by funding from the Marine diversity in marine benthic ecosystems: a comparison of Institute at the University of Plymouth and the Devon Wildlife approaches. Mar Ecol Prog Ser. 254(2):11–25. Trust as well as the NERC’s Oceans 2025 programme. Thanks Bremner J, Rogers SI, Frid CLJ. 2006a. Matching biological traits to Dr Tim Stevens, Griffith University, Australia, for providing to environmental conditions in marine benthic ecosystems. J the species matrix data; Dr Emma Jackson, Dr Olivia Langmead Mar Syst. 60(3–4):302–316. and Charlotte Marshall, University of Plymouth and MarLIN; Bremner J, Rogers SI, Frid CLJ. 2006b. Methods for describ- and Dr Harvey Taylor-Walters, Marine Biological Association for ing ecological functioning of marine benthic assemblages advice on this research and Dan Lear and Becky Seeley, DASSH, using biological traits analysis (BTA). Ecol Indic. 6(3): for providing Seasearch data. We also thank the two anonymous 609–622. reviewers for their valuable and constructive input. Bulling MT, Hicks N, Murray L, Paterson DM, Raffaelli D, White PCL, Solan M. 2010. 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Journal

International Journal of Biodiversity Science, Ecosystem Services & Management – Taylor & Francis

Published: Sep 1, 2012

Keywords: biological traits analysis; ecosystem function; MPA; marine spatial planning; service-orientated framework

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