Current state of seagrass ecosystem services: Research and policy integration

Ocean & Coastal Management 149 (2017) 107e115

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Current state of seagrass ecosystem services: Research and policy integration
a A. Ruiz-Frau a, *, S. Gelcich b, I.E. Hendriks a, C.M. Duarte c, N. Marba Department of Global Change Research IMEDEA (CSIC-UIB), Miquel Marqu es 21, 07190 Esporles, Spain Center of Applied Ecology and Sustainability & Laboratorio Internacional en Cambio Global, Facultad de ciencias biologicas, Pontificia Universidad Catolica de Chile, Chile c King Abdullah University of Science and Technology (KAUST), Red Sea Research Center (RSRC), Thuwal, 23955-6900, Saudi Arabia a

b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 3 May 2017 Received in revised form 19 September 2017 Accepted 1 October 2017

Seagrasses contribute to the maintenance of human wellbeing. However certain aspects of their role as ecosystem service (ES) providers remain understudied. Here, we synthesise the state of seagrass ES (SGES) research and policy implications. Additionally, we recommend ways in which SGES research can be integrated in to policy design, by drawing lessons from the case of Blue Carbon (BC). SGES research suffers from three main biases: a geographical bias, SGES has been restricted to chartered seagrass areas; a type of service research bias, provisioning and regulating services have received extensive attention while cultural services remain understudied; a type of discipline bias, the ecological aspects of SGES have been well documented while economic and social aspects remain in comparison understudied. These are particularly important, as an understanding of the social and economic considerations of the provision of ES is fundamental to facilitate its integration into policy frameworks. Lessons drawn from the operationalization process of BC show the reoccurrence of certain aspects that have enabled the integration of BC into policy. These aspects are grouped under 4 different categories. From the analysis of these elements we draw lessons that could facilitate the operationalization of other ecosystem services and their incorporation into management policy frameworks. © 2017 Published by Elsevier Ltd.

1. Introduction Ecosystems provide essential goods and services supporting human health, livelihoods, wellbeing and survival, these have been termed ecosystem services (ES) (MEA, 2005). Over the last two decades the ecosystem services concept has emerged as a major framework for discussing social-economic-ecological interactions, sparking growing interest in both research and policy arenas (Braat and de Groot, 2012). The debate on ES and their value to humans was initiated by a first attempt at quantifying the global value of ES (Costanza et al., 1997). The momentum of the ES concept increased subsequently with the publications of the United Nations' Millennium Ecosystem Assessment report in 2005 (MEA, 2005) and The Economics of Ecosystems and Biodiversity report in 2010 (TEEB Foundations, 2010). These international initiatives highlighted the relationships between ecology and economy, the importance of ES

* Corresponding author. E-mail address: [email protected] (A. Ruiz-Frau). https://doi.org/10.1016/j.ocecoaman.2017.10.004 0964-5691/© 2017 Published by Elsevier Ltd.

and the consequences of ecosystem changes for human wellbeing. Valuation approaches have been crucial in revealing the value of ES to humans and in their integration into policy. Although the value of ecosystems to human wellbeing has many dimensions -sociocultural, ecological and economic- and can be expressed in a range of units (e.g. energetic, land, time), monetary units have been predominantly chosen above the rest. This choice has often been criticised as some consider that this approach implies the “commodification” of nature (McCauley, 2006; Gomez-Baggethun and Ruiz-Perez, 2011) arguing that nature should be valued by its intrinsic value and not by human allocated utilitarian values. Nevertheless, the use of monetary units represents a pragmatic choice as it resonates with dominant political and economic views and serves best to communicate to different audiences (de Groot et al., 2002; Daily et al., 2009). Ocean and coastal ecosystems have been estimated to contribute to more than 60% of the total economic value of the biosphere (Costanza, 1999; Martinez et al., 2007; Costanza et al., 2014). Yet, despite their importance, data and methods to assess ocean and coastal ecosystem services are lagging behind those of

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2. Methodology

the other on seagrass ecosystem functions. The first search included those studies which contained the terms seagrass* AND “ecosystem service*” in the title, abstract or keywords. This search resulted in a total of 165 documents. To ascertain the relevance of the studies, abstracts of the 165 records were screened. For those studies in which the abstract was not sufficient to determine the study content, the full text of the article was assessed. Articles (62%) were excluded if they were either not related to SGES or if they used the term ecosystem service only as justification for the study without assessing SGES. The remaining 62 studies were retained for further analyses. Services were classified according to the classification established by The Economics of Ecosystems and Biodiversity (TEEB) (Brink et al., 2009). Information on the main characteristics of the studies was extracted: publication year, perspective (ecological, economic, social, mixed), analysis type (quantitative, qualitative, conceptual, mixed), number and type of services assessed, type of data (primary data, review data, model data, proxy data, mixed sources), spatial scale (local, subnational, national, supranational, continental, global, laboratory experiment) and geographical coordinates. It was considered that a paper adopted an ecological perspective when it focused on measuring ecological functions or ecosystem properties, an economic perspective when the study focused on the estimation of use or non-use values of SGES and/or their associated benefits in monetary terms and a social perspective if the paper focused on the values people attributed to SGES and/or their associated benefits. The second search was performed to obtain publications on the seagrass functions underlying each of the services attributed to seagrasses: food provision, gas and climate regulation, disturbance prevention, lifecycle maintenance, nutrient removal, leisure and pharmaceutical benefits. The search terms used for the different services are detailed in Table 1. A total of 1551 records were obtained, which abstracts were screened in order to quantify the number of relevant studies within each ecosystem function category (Table 1). Studies were included in the analysis only when the seagrass function under study was assessed, studies which only mentioned a particular seagrass function in the title, abstract or keywords without including some type of quantitative or qualitative analysis in the main body of the article, were excluded. A list of all the articles included in the analyses is available as SI. Additionally, to analyse the case of BC and discuss the elements that enabled its integration into policy a search for peer-reviewed and grey literature was performed. Peer-reviewed literature was retrieved using the search term “blue carbon” in Web of Science between 1864 and 16.06.2016. Document type was restricted to article or review. This search resulted in a total of 180 documents. Abstracts were screened to ascertain their relevance. Articles were excluded if they were not related to BC in marine or coastal ecosystems. A total of 73 articles were retained for further analysis. Grey literature was obtained through specific BC repository web sites such as the bluecarbonportal.org.

2.1. Literature search

3. Results

We compiled studies on seagrass ES published in the peerreviewed literature between 1864 and 16.06.2016 using Web of Science. Document type was restricted to article or review. Grey literature and non-English publications were omitted from the search. Since a considerable number of publications relevant for SGES focussed on ecological functions or on socioeconomic aspects without mentioning the term service, which was introduced in the late 1980's, we conducted two searches using different sets of keywords. One search focused on seagrass ecosystem services and

3.1. Seagrass ecosystem services

terrestrial systems (Barbier, 2012; TEEB, 2012), especially when it comes to mapping, modelling and valuating ES (Barbier, 2012; Maes et al., 2012; Liquete et al., 2013). The absence of detailed spatial information on habitat distribution and the difficulties in quantifying both functions and processes in the marine environment are considered the main causes for these differences (Maes et al., 2012). Within coastal systems, seagrasses are key components that provide crucial ecosystem services. Seagrasses occur along the shores of all continents (except Antarctica) to a maximum depth of 50 m (Hemming and Duarte, 2000). Seagrasses contribute to the protection of coastal areas by protecting the shoreline (Boudouresque et al., 2016), diminishing wave energy and trapping sediments (Ondiviela et al., 2014), providing important nursery areas for a range of fish, shellfish and crustacean species (de la Torre-Castro and Ronnback, 2004; Jackson et al., 2015; Whitfield, 2017), regulating the cycling of nutrients (Costanza et al., 2014) and playing a significant role in the global sequestration and burial of carbon (Kennedy et al., 2010; Fourqurean et al., 2012; Duarte et al., 2013a), among others. Although no comprehensive data on the global distribution of seagrasses exists, the most commonly used estimates in the literature use a lower estimate of 150,000 km2 and a high estimate of 600,000 km2 (Duarte, 2005; Nellemann et al., 2009; McLeod et al., 2011). Regrettably, despite their ecological and societal importance, it is estimated that seagrasses are being lost globally at rates of about 5e7% year
1. It is also estimated that only in the last seventy years one third of seagrass coverage has been lost (Orth et al., 2006; Waycott et al., 2009). The increased knowledge on the important role played by seagrasses in the capture and storage of carbon (Duarte et al., 2005) has led to the proposal that seagrasses together with mangroves and saltmarshes systems can significantly contribute to climate regulation and should be part of climate change mitigation policies (McLeod et al., 2011; Nellemann et al., 2009). Carbon sequestered and stored by these systems has been termed Blue Carbon (BC) (Nellemann et al., 2009). BC is currently being considered into regional and national environmental management policies, offering an opportunity to analyse aspects that have enabled the successful integration of this specific seagrass ES into international policy. In other words, the success story of BC provides the opportunity to identify those elements that have led to the operationalization of the ES concept. Here we synthesise the state of seagrasses ecosystem services (SGES) research and policy implications. Our purpose is to: (1) undertake a systematic evaluation to assess the temporal evolution and state of research on SGES, (2) identify key topics on SGES that are yet to be addressed by the research community, and (3) recommend ways in which SGES research can be better integrated into policy design, by drawing lessons from the case of BC. A main goal of this evaluation is to identify critical research gaps that need to be incorporated into future research agendas to enable the operationalization of the ES concept to support the sustainability of seagrass meadows.

The term ecosystem service related to seagrasses was first used in a scientific publication in 1997 by Costanza et al. in a paper where marine and terrestrial ES were economically valued, although it was not until 2000 (Duarte, 2000) when a publication specifically focused on SGES was published, almost 20 years after the first peer-reviewed scientific publications on general ecosystem services appeared in 1983 (Ehrlich and Mooney, 1983; Myers, 1983).

A. Ruiz-Frau et al. / Ocean & Coastal Management 149 (2017) 107e115 Table 1 Search terms used in the evaluation of papers on seagrass functions underlying the provision of services. Service

Search terms: Seagrass* AND …

N results

% relevant results (N)

Food provision Gas & climate regulation

Fisheries “carbon storage” OR “carbon burial” OR “carbon sequestration” OR “carbon stock” OR “carbon sink” “coastal protection” OR “coastal erosion” OR “particle trapping” OR “particle retention” OR “wave attenuation” OR “flow modification” nursery OR “feeding ground*” “nutrient sink” OR “nutrient removal” “leisure” OR “recreation” pharmaceut*

578 72

14% (84) 67% (48)

160

45% (72)

585

45% (265)

105

32% (34)

43

6% (3)

8 1551

88% (7) 513

Disturbance prevention

Lifecycle maintenance Nutrient removal Leisure Pharmaceutics Total number of articles

In Web of Science the asterisk (*) is used as a wildcard and represents any group of characters, including no character.

The use of the term SGES increased exponentially since then, approximately 63% of the studies assessed any of them (Fig. 1A). The annual rate of increase of publications on SGES is similar to that of marine and coastal ecosystem services (MCES) and general ES (Fig. 1B). At present, publications on SGES represent 2% of publications on general ES and 19% of publications on MCES, with an annual rate of increase of 4% and 11% respectively since 1998. Publications on SGES represent 2.3% of publications on the field of seagrass ecology and biology but this percentage has changed over the last two decades, increasing at an annual rate of 26% (Fig. 1C). The approach of 63% of the studies included some type SGES quantification (Fig. 2A), most were of an ecological nature (45%), the rest adopted an economic (21%) or mixed (21%) perspective. Mixed studies generally offered a combination of ecological and economic valuations. In general, qualitative studies (13% of the total) offered a social perspective of the value of seagrasses for local communities, 75% of these studies adopted either a purely social perspective or a combined social-ecological approach. A small proportion of the records (11%) included in the evaluation focused

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on the development of novel conceptual frameworks that included SGES in their structures. Almost 50% of the studies collected their own data, 19% were based on data from previous studies, 16% presented data derived from models and the rest used data from mixed sources. In general, studies did not focus on the assessment of a single ecosystem service but rather assessed multiple services, the average number of which was 2 per paper. Approximately 21% of the papers focused on seagrasses as a food provisioning habitat, most studies on this area adopted a social valuation approach such as in the assessment of the importance of seagrasses as low tide gleaning and artisanal fisheries areas for local communities (Table 2). Regulating services received the most attention (65% of the studies), followed by supporting services (42%) (Fig. 2B). Cultural services conversely have remained understudied (19% of the studies assessed cultural services). Within the regulation category, the role of seagrasses in climate regulation through the sequestration and storage of carbon has received the most attention (35%), followed by their contribution to the protection of coastal areas by reducing wave energy and stabilising the sediment (24%). In the supporting services category, most attention has been focused on the importance of seagrasses as nursery areas for juvenile fish species (27%). Research on the maintenance of good water quality has centred on their role in nutrient cycling, especially nitrogen (N) and phosphorous (P) (15%). For provisioning, regulating and supporting services most studies have focused on the ecological assessment of the services, while their economic and social aspects, such as their contribution to coastal protection for local communities, have received less attention. Only a small portion of articles assessed seagrasses as providers of cultural services (Table 2). Geographically, empirical studies on SGES have mainly focused on North America, Europe, the southern coast of Asia and AustraliaOceania (Fig. 3). In North America, where the highest number of studies has been recorded (12), studies were mainly of an ecological nature (58%). Ten studies were located around European coasts, half of them adopted an economic approach for the assessment of SGES. A total of 7 studies were recorded in Asia, 71% assessed SGES from an ecological perspective while the rest adopted a combination of an ecological-economic-social approach. Few studies were recorded for South America, the West and South coasts of Africa or the northern coasts of Europe. A total of 14 studies adopted a more general perspective on SGES without referring to specific geographical locations, drawing conclusions with global applications.

Fig. 1. Temporal evolution of publications on seagrass ecosystem services (SGES); (A) total number of publications containing the term SGES and number of real SGES publications (those assessing SGES in some form); (B) Annual rate of increase of publications on ES in general, marine and coastal ES (MCES) and SGES; (C) Proportional annual rate of increase of publications on SGES relative to that of ES in general, MCES and general publications on seagrasses. Dashed lines in panels B and C indicate the fitted regression equations between the natural log of the corresponding cumulative number of publications and time, i.e. the increase rate of publications, which is the slope of the fitted equation multiplied by 100, is shown next to each dashed line. Searches for MCES and ES in general were performed through Web of Science using the search terms (“ecosystem service*” or “environmental service*”) and (“marine” or “sea” or “ocean”) for MCES and (“ecosystem service*” or “environmental service*”) for ES in general.

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Fig. 2. (A) Distribution of seagrass ecosystem services (SGES) studies according to study type and approach adopted; (B) Distribution of SGES studies according to service type.

Table 2 Number of studies published on the different ecosystem services provided by seagrasses and proportions of ecological, economic and social studies for each of them. Total percentages do not add to 100% since some studies assessed more than one ES at a time.

Provision Food Raw materials Regulation Gas & climate regulation Coastal protection Bioremediation of waste Support Lifecycle maintenance, habitat & gene pool protection Water condition Cultural Research & education Recreation & tourism Cultural heritage & identity Total (%)

N

Ecological (%)

Economic (%)

Social (%)

Mixed (%)

9 4

22

33 75

22 50

11 50

22 15 3

59 33 33

14 27 33

23 20 33

17

71

12

18

9

44

22

11

4 6 2

25 17

50 33

25 17 50

17 50

50%

21%

6%

27%

3.2. Seagrass ecosystem functions The search focusing on seagrass ecosystem functions (SEF) underlying the provision of services retrieved a total of 513 publications. This figure was 8 times greater than the number of publications on seagrasses explicitly mentioning the term “service” (Fig. 1, Table 1). With the exception of publications on the nursery role played by seagrasses, which started in 1978, publications on the functions of seagrasses started circa 1990, almost 10 years before the term “seagrass ecosystem service” was first used (Fig. 4). Publications that would qualify as nursery service, on the provision of food and habitat and inventories of juvenile and adult stages of fish and shellfish species on seagrasses have by far received the greatest attention (Fig. 4). Since 1978, 265 studies on this topic have been published; this represents fifty-one per cent of the total number of publications on SEF collected for this evaluation. Seagrasses have also received particular attention as food

provisioning areas for humans, with a focus on the adult stages of fish and shellfish species associated with seagrass meadows. In particular, studies focussed on their importance for small-scale fisheries and their role as a source of biomass for fisheries, as a considerable number of commercial species spend part of their life cycle in seagrass meadows (Jackson et al., 2015). Over the past ten years there has been a significant increase in publications on the role of seagrasses in coastal protection, the sequestration and storage of carbon and their function in nutrient removal of nutrients from the water column (Fig. 4). A steady increase in papers on coastal protection has occurred since year 2000 with an annual rate of increase of 21%. Papers on this topic have mainly focused on the effects of seagrass meadows on wave attenuation (35% of publications) and buffering sediment erosion (19%). Approximately 17% of the publications considered the subject from a more general perspective considering all the different factors that play a role in the protection and maintenance of the coasts. Publications on the removal of nutrients from the marine environment have mainly (94%) focused on plant nutrient dynamics (uptake, the fate of nutrients in seagrass tissues) and sediment nutrient fluxes and stocks at short time scales (1 year). Only few (6%) studies assessed long-term nutrient burial in seagrass meadows (Mateo et al., 1997; Gonneea et al., 2004). The annual average number of publications is low, less than two publications per year. Yet, the effort allocated to assess nutrient dynamics in seagrass meadows varied over the last 3 decades, growing at 30% yr
1 during the 90's, slowing down to 4.3% yr
1 between years 2002 and 2011 and with only 2 publications on the topic found between 2012 and 2016 (Fig. 4). Very few studies were found on the pharmaceutical applications of compounds extracted from seagrasses. Seven publications were released between 2005 and 2016, on the anti-inflammatory, antioxidant, immunostimulatory and anti-tumour properties of certain seagrass substances.

3.3. Blue carbon Peer-reviewed scientific publications on the carbon cycle functions of seagrasses, including carbon sequestration, storage and

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Fig. 3. Geographical and disciplinary bias of seagrass ecosystem services studies. Dots indicate the location of studies done at specific sites; the rest of studies adopted a global or general approach to SGES (histogram on Southern Ocean).

the total number of publications on BC focused on seagrasses. Of those, 67% adopted an ecological perspective, 9% an economics perspective, 6% a combination of the previous two and 24% focused on the policy aspect and the integration of BC into management.

4. Discussion 4.1. Evaluation of seagrass ecosystem services research

Fig. 4. Temporal evolution of publications on the seagrass functions underlying the provision of services. Numbers in brackets represent the average increase in the annual rate of publications.

sink capacity were initiated in 1995 (Fig. 4), although Smith already highlighted the important role of marine macrophytes in general as carbon sinks in 1981 (Smith, 1981). Twelve studies were published between 1992 and 2008, at a modest average rate of 1.3 publications per year. However, over the past eight years (2009e2016) the number of publications has quadrupled, with an average annual publication rate of 5 papers. This increase in publication numbers has coincided with the release of a United Nations landmark report highlighting the role of seagrasses, tidal saltmarshes and mangrove systems, which the authors termed Blue Carbon (BC) habitats, as intense carbon sinks (Nellemann et al., 2009). The first peerreviewed publication to use the term BC appeared in 2011 (McLeod et al., 2011), since then the publication rate of seagrass BC has increased exponentially. Between 2011 and 2016, almost 80 publications on BC (including seagrasses, mangroves and saltmarshes) have been published in ecology, management and policy related scientific journals. The interest in and relevance of the role of BC is reflected on the rapid growth of publications, which has experienced an annual increase rate of 85%. Approximately 42% of

The field of seagrass ecosystem services research is a relatively novel research area, initiated after Costanza et al. (1997) ranked seagrasses amongst the most valuable biomes on Earth. However, specific research into seagrass ecosystem services is a relatively novel program that appeared around 2008, following an almost complete void in addressing SGES in peer-reviewed journals. This might be partly attributable to the fact that academics focusing on seagrass research seldom write about their findings adopting an ES framework. Similar patterns can be observed in publications on marine and coastal ES (Liquete et al., 2013) or on ES in general. We identified here several important knowledge gaps in the assessment of SGES. Three main information biases have been detected, namely a geographical bias, a service bias and a disciplinary bias. Geographically, studies on SGES have mainly, but not exclusively, concentrated along the coasts of North America, the southern coast of Asia and the coasts of Australia-Oceania, leaving great portions of coastal areas virtually un-assessed, this is comparable to the findings in Nordlund et al. (2016). There is a need to expand existent research into the coastal areas of Southeast Asia, the eastern and western coast of South America and the West coast of Africa in order to obtain a more accurate picture of the global magnitude of ES provided by seagrasses. These areas mainly coincide with unsurveyed areas for which the extent of seagrass coverage is largely unknown (Duarte et al., 2013a). Thus, it seems that the geographical bias in SGES research is heavily linked to uncertainties on the regional extent of seagrass meadows. So far, limitations in the use of remote sensing tools have precluded the

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reliable estimation of seagrass cover. However, a recent review on the application of remote sensing techniques to seagrass ecosystems reveals substantial advances in seagrass detection, assessment of areal coverage, distribution, mapping and the detection of the extent of biomass changes (Hossain et al., 2015). The mapping of currently unsurveyed seagrass areas and the development of a critical number of SGES assessments around the world would allow the estimation of the global magnitude of SGES provision and how these maybe affected by different climatic, conservation and management scenarios. Our analysis revealed an unbalance in the type of services assessed. Regulating and provisioning services have received considerable attention (37% and 63% of the total number of publications, respectively) and although there are still important knowledge gaps, the amount of existing information on services such as carbon sequestration, coastal protection and seagrasses as fisheries or nursery areas is sufficient to allow SGES to be integrated into policy frameworks. There has been a clear tendency towards the assessment of the ecological aspects of SGES and the functions underpinning them. In terms of coastal protection services, efforts have been directed towards demonstrating the role of seagrasses as providers of coastal protection (Ondiviela et al., 2014). Morphologically, seagrasses are flexible, especially compared to other coastal vegetation like salt marshes and mangroves. Therefore, their impact on wave attenuation and sediment accretion would be limited compared to stiffer vegetation types (Bouma et al., 2005). However, they play a major role in reducing coastal erosion and in trapping and retaining of eroded sediment (Gacia and Duarte, 2001; Madsen et al., 2001), which is still poorly quantified. Sediment accretion, even over longer timescales, can play a role in prevention of flooding, relevant for climate change adaptation at the current rate of sea level rise (Borsje et al., 2011). It has been shown that seagrasses cannot always provide adequate coastal protection services and their risk reduction services are context dependent (e.g. geomorphology, hydrodynamics, conservation state). Hence, coastal protection services cannot be readily extrapolated across coastal locations and should be quantified at the site level (Ondiviela et al., 2014). The carbon sequestration and storage services provided by seagrasses (Blue Carbon, BC) has also been the focus of increasing research efforts. The realization in 2005 that seagrass ecosystems are globally-significant carbon sinks (Duarte et al., 2005), coinciding with the publication of the Millennium Ecosystem Assessment and followed by the appearance of the term BC in 2009 (Nellemann et al., 2009), provided a substantial momentum for the focus on seagrass ecosystems as carbon sinks. Recent findings have identified them as intense carbon sinks that can store up to 25 to 132 gCm
2 yr
1, exceeding the sequestration capacity of rainforests, and hold that carbon over millenary time scales (Kennedy et al., 2010; McLeod et al., 2011; Fourqurean et al., 2012; Duarte et al., 2013b, 2013c). However, there are still uncertainties that need to be addressed. To fully comprehend the magnitude of the carbon sink capacity of seagrasses it is necessary to understand carbon stocks and burial rates over different time scales, the fate of carbon exported from meadows, the variability in sink capacity and the fate of carbon stocks following disturbance and seagrass loss (Duarte et al., 2013a). Nevertheless, despite these knowledge gaps there is sufficient understanding on the mechanisms underpinning the sequestration and storage of seagrass BC and evidence that the restoration and conservation of BC habitats can be effective strategies for climate change mitigation (Marba et al., 2015). Collectively, the scientific knowledge of the role of BC is sufficiently robust to enable the integration of BC into policy frameworks. Therefore, a sound scientific understanding of the ecological processes that support the provision of ecosystem services is crucial to

allow operationalization. The analysis shows that cultural services associated to seagrasses have remained understudied albeit the fact that they provide substantial opportunities for recreation, artistic inspiration, research and education (Garcia Rodrigues et al., 2017). The assessment of cultural heritage and identity values is also of particular importance, especially around coastal rural communities that tend to depend to some extent on the services provided by seagrasses (de la Torre-Castro and Ronnback, 2004; Cullen-Unsworth et al., 2014). The third knowledge gap identified during this evaluation relates to a disciplinary bias (i.e. scope of the studies) in the assessment of SGES. Half of the papers adopted an ecological approach in the assessment of SGES, while only 21% and 6% assessed SGES from a purely economic and social perspective, respectively. However, 27% adopted a combination of the three disciplines in the assessment of SGES. There is a need to increase and direct research efforts towards the assessment of these two aspects of SGES. As an example, information on the economic value of the coastal protection services offered by seagrasses remains insufficient. Yet, economic valuation is fundamental if seagrass ecosystems are to be included in risk reduction plans as it allows the integration of natural and man-made solutions for coastal protection in hybrid cost-benefit analyses (Bouma et al., 2014; Spalding et al., 2014). Dewsbury et al. (2016) argue that existing valuation frameworks for seagrasses are very limited and incomplete, since models tend to ignore the quality of the meadows and the effect it might have on the provision of services (e.g. TESSA (Peh et al., 2013), InVEST (Guerry et al., 2012)). Recently however, a framework for valuation of SGES has been suggested where ecological and economic relationships and the different goods and services provided by seagrass ecosystems can be delineated individually, therefore allowing prediction of how seagrasses might function under different scenarios (Dewsbury et al., 2016). There is a need to increase the number of studies focused on the social valuation and importance of SGES for different types of communities. This study evidenced the lack of knowledge on this particular area of SGES assessments, the shortage of information on the social relevance of ES seems to be a common deficiency in the assessment of ES in general, not being only restricted to SGES (Liquete et al., 2013; Thomas, 2014). Social aspects are particularly relevant in cases of ES marketization as the governance and perceptions of the demand and supply of ES are critical elements for their success (Gelcich and Donlan, 2015). Social aspects might be especially complex in the case of marine and coastal areas as they are subject to different types of tenures, management and ownership rights that differ from those on land (e.g. open access, coastal community rights, customary access to fishing grounds) both in developed and traditional societies (Hastings et al., 2012). These unique characteristics require the expansion of current social research in order to comprehend the governance systems around marine and coastal ecosystem services in general and on seagrass ecosystem services in particular. A major bottleneck in the social valuation of SGES is the insufficient public awareness on seagrasses (Cullen-Unsworth and Unsworth, 2016). This insufficient knowledge weakens the foundations for societal appreciation of SGES. 4.2. Blue carbon example The examination of the story of Blue Carbon (among others Gordon et al., 2011; Herr and Laffoley, 2012; AGEDI, 2013; BCP, 2015) indicates the reoccurrence of aspects that might play an important role in facilitating the integration of BC into policies. We argue that crucial aspects for this integration have been: (i) the existence of a critical threshold of scientific knowledge regarding

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the capture and storage of carbon, as indicated here; (ii) the involvement of international non-governmental organizations and agencies in the development of BC initiatives and demonstration projects; (iii) the analysis of ways to operationalize BC into policy frameworks and the de-facto incorporation through pioneering examples and (iv) the integration of BC into finance mechanisms. In contrast to the underrepresentation of social and economic studies on the diverse range of SGES, in the case of BC for coastal vegetated habitats the development of a significant and growing number of BC demonstration projects by a range of countries and organizations around the world has greatly contributed to bridge the existing gap in social and economic research. Demonstration projects have not only shown how the incorporation of carbon and other ES values into local and national financial markets and coastal management plans can ensure the long-term protection of BC ecosystems but they also highlight the direct benefits for communities living in vulnerable areas from climate change related threads (e.g. flood prevention, erosion control) (Rao et al., 2012; GEF IW:LEARN, 2015; Livelihoods, 2015). Two examples of demonstration projects are the Blue Forests project and the Livelihood Funds. The Blue Forest programme is a four-year multimillion project implemented by UNEP, which aims at pushing the BC (or blue forest) concept from theory to practical application. Project activities started in 2014 and are under way in Indonesia, Madagascar, Mozambique, Ecuador and the United Arab Emirates (GEF IW:LEARN, 2015). The Livelihood Funds project focuses on the protection of vulnerable areas and communities from climate change related threads through the restoration of coastal vegetated habitats. This initiative has already restored close to 17000 ha of mangroves which are expected to offset around 1.2 millions tonnes of carbon while protecting local communities from coastal erosion (Livelihoods, 2015). The execution of this range of BC demonstration projects has been partly possible through the interest, involvement and financial support of international agencies and organizations such as IUCN, CI, UNEP, FAO, IOC, UNESCO,1 or Wetlands International. The financial support and interest of these NGO's and agencies has been crucial in the global acknowledgement of the importance of vegetated coastal habitats as ES providers. Examples of publications by these organizations are landmark reports such as the publication in 2009 of the UNEP report “Blue Carbon: A rapid response assessment” (Nellemann et al., 2009), where the term BC was coined, and the importance of BC habitats highlighted as significant elements in climate change mitigation. Likewise, the publication of a Blue Carbon Initiative report outlining options to include BC into policy (Herr and Laffoley, 2012) has facilitated the integration of BC into several policy frameworks (AGEDI, 2013; NOC, 2013; CCPR and NRWG, 2014). Abu Dhabi's Blue Carbon Demonstration project (AGEDI, 2013) serves as an example for the incorporation of BC in national policy frameworks, as BC has been integrated into Abu Dhabi's National Biodiversity Strategies and Action Plans, National Performance Indices, National Climate Change programmes and urban development plans (AGEDI, 2013). In the US, NOAA (National Oceanographic and Atmospheric Administration) is developing guidance to incorporate ecosystem services, and BC in particular, into federal policies by changing the way policies are implemented to include the carbon services of habitats (Pendleton et al., 2013; Sutton-Grier et al., 2014). On a practical level, in April 2013 the White House released the National Ocean Policy Implementation

1 International Union for Conservation of Nature (IUCN), Conservation International(CI), United Nations Environment Program (UNEP), the Food and Agriculture Organization (FAO), the Intergovernmental Oceanographic Commission (IOC), the United Nations Educational, Scientific and Cultural Organization (UNESCO).

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Plan (NOC, 2013) where carbon capture and storage is included as one of the important services provided by coastal ecosystems. More recently, in October 2014 as part of the Priority Agenda on Enhancing the Climate Resilience of America's Natural Resources (CCPR and NRWG, 2014) released by the US Council on Climate Preparedness and Resilience, NOAA and FWS (Fish and Wildlife Service) established the identification and support of key restoration projects that can increase coastal BC sinks. These examples offer the initial steps of the integration of an important ES into policy frameworks that will eventually conduct towards the maintenance of coastal vegetated habitats. One might argue that some of the crucial elements that have enabled the integration and operationalization of BC, as opposed to the rest of SGES, (i.e. bridged gap in social valuation studies, execution of demonstration projects and involvement and support of international agencies) have only been possible through the existence of one crucial element which is missing for the rest of ES, that is, the existence of a financial framework that has enabled the marketization of BC. Currently, two main options exist for the marketization of BC, financing through the UNFCCC (United Nations Framework Convention on Climate Change) and the integration into alternative finance mechanisms such as voluntary carbon markets. However, most financing mechanisms only include mangrove ecosystems in their frameworks. In order to promote the inclusion of the rest of BC ecosystems (i.e. saltmarshes and seagrasses), non-forested marine and coastal systems should be included in their regulations (Wylie et al., 2016). Additionally, an option that might further incentivise the protection and restoration of these ecosystems could be the creation of a framework that would allow the marketization of other services besides BC. Some SGES such as the contribution of seagrasses to fisheries production are already embedded within financial markets through the commercialisation of fish. Other services however, e.g. coastal protection or nutrient removal, which benefits are experienced at local scales (in opposition to the global benefits of carbon sequestration) and might not be as easily tradable (as in the case of fish) might need alternative mechanisms to facilitate their operationalization. Mechanisms such as cost-benefit analyses (CBAs), where not only economic but also sociocultural valuations of ES would need to be included, could become necessary elements within legal frameworks for any actions that might affect the integrity of the environment. Such instruments are already part of national environmental guidelines in countries like Norway (NGA, 2016) and could promote the integration and operationalization of the ES concept. However, CBAs should only be part of an array of different mechanisms to fully capture the value of ES, as the value of some services such as socio-cultural services, might not be easily reflected through the use of this particular tool. Their use in combination with frameworks like Multi-Criteria Decision Analysis (MCDA) frameworks could deliver a broader set of ES values, including those related to sociocultural services (Saarikoski et al., 2016). 5. Conclusion The operationalization of SGES will most likely go through the fulfilment of the three knowledge gaps identified in this evaluation (i.e. geographical, type of service and discipline biases). There is a need to expand SGES research into areas such as the coasts of South America, Southeast Asia and the West coast of Africa. The lack of information on SGES is strongly linked to the incomplete information on the current global extent of seagrasses. Provisioning and regulating services have received extensive attention while fewer research efforts have been dedicated to cultural services. Similarly, the ecological aspects of SGES have been well documented while

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the economic and particularly the social aspects of SGES remain understudied. The analysis of the operationalization process of BC has shown that one of the aspects where BC is substantially further in comparison to marine and coastal ES research is the understanding of the social aspects associated to the provision and demand of services which has been mostly achieved through demonstration projects performed in different parts of the world. Research into the highlighted areas will be fundamental to the acknowledgement of the significance of the benefits of SGES for human wellbeing and will thus facilitate their integration into policy frameworks. The analysis of the operationalization of BC has shown crucial factors that have enabled BC integration into policy frameworks, which could be used as a model for the operationalization of services derived from other ecosystems. A sound understanding of the ecological processes underpinning the service; the involvement of international agencies; the development of projects that demonstrate not only the ecological but also the economic and social benefits of maintaining the provision of ES and the existence of marketization mechanisms might be fundamental pieces in the integration of ES into policy. Acknowledgements The authors would like to genuinely thank the contribution of the anonymous reviewers whose suggestions greatly improved the quality of the present publication. Funding: this study was funded by the EU FP7 OPERAs (contract no. 308393). Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.ocecoaman.2017.10.004. References AGEDI, 2013. Blue Carbon in Abu Dhabi- Protecting Our Coastal Heritage. The Abu Dhabi Carbon Demonstration Project. Barbier, E.B., 2012. Progress and challenges in valuing coastal and marine ecosystem services. Rev. Environ. Econ. Policy 6, 1-þ. BCP, Blue Carbon Portal(CCPR and NRWG, 2014), 2015. Mikoko Pamoja Mangrove Reforestation, Kenya. Borsje, B.W., van Wesenbeeck, B.K., Dekker, F., Paalvast, P., Bouma, T.J., van Katwijk, M.M., de Vries, M.B., 2011. How ecological engineering can serve in coastal protection. Ecol. Eng. 37, 113e122. Bouma, T.J., De Vries, M.B., Low, E., Peralta, G., Tanczos, C., Van de Koppel, J., Herman, P.M.J., 2005. Trade-offs related to ecosystem engineering: a case study on stiffness of emerging macrophytes. Ecology 86, 2187e2199. Bouma, T.J., van Belzen, J., Balke, T., Zhu, Z., Airoldi, L., Blight, A.J., Davies, A.J., Galvan, C., Hawkins, S.J., Hoggart, S.P.G., Lara, J.L., Losada, I.J., Maza, M., Ondiviela, B., Skov, M.W., Strain, E.M., Thompson, R.C., Yang, S., Zanuttigh, B., Zhang, L., Herman, P.M.J., 2014. Identifying knowledge gaps hampering application of intertidal habitats in coastal protection: opportunities & steps to take. Coast. Eng. 87, 147e157. Boudouresque, C.F., Pergent, G., Pergent-Martini, C., Ruitton, S., Thibaut, T., Verlaque, M., 2016. The necromass of the Posidonia oceanica seagrass meadow: fate, role, ecosystem services and vulnerability. Hydrobiologia 781, 25e42. https://doi.org/10.1007/s10750-015-2333-y. Braat, L.C., de Groot, R., 2012. The ecosystem services agenda:bridging the worlds of natural science and economics, conservation and development, and public and private policy. Ecosyst. Serv. 1, 4e15. Brink, P., Berghofer, A., Schroter-Schlaack, C., Sukhdev, P., Vakrou, A., White, S., Wittmer, H., 2009. TEEB - the Economics of Ecosystems and Biodiversity for National and International Policy Makers- Summary: Responding to the Value of Nature 2009. CCPR and NRWG, 2014. Page 79. In: U. S. Council on Climate Preparedness and Resilience and Natural Resources Working Group (Ed.), Priority Agenda Enhancing the Climate Resilience of America's Natural Resources (Washington D.C.). Costanza, R., 1999. The ecological, economic, and social importance of the oceans. Ecol. Econ. 31, 199e213. Costanza, R., dArge, R., deGroot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K.,

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