North Atlantic coastal lagoons: conservation, management and ...

Hydrobiologia (2013) 701:1–11 DOI 10.1007/s10750-012-1325-4

OPINION PAPER

North Atlantic coastal lagoons: conservation, management and research challenges in the twenty-first century Nicola A. Beer • Chris B. Joyce

Received: 10 May 2012 / Revised: 20 August 2012 / Accepted: 10 September 2012 / Published online: 23 September 2012 Ó Springer Science+Business Media Dordrecht 2012

Abstract Coastal lagoons provide socio-economically valuable ecosystem services and are important habitats for conservation. Rare around North Atlantic coastlines, they are increasingly threatened by climatic and anthropogenic stressors. Despite repeated calls at the end of the twentieth century for further research to be urgently undertaken to underpin management of these habitats and the rare, specialist species they support, progress on North Atlantic lagoons has apparently lagged behind other European lagoon types. In the context of increasing pressure on coastal resources, we summarise current ecological knowledge and consider contemporary issues, concepts and techniques to identify the conservation, management and research challenges that need to be addressed if North Atlantic lagoons are to be safeguarded and sustainably managed in the twenty-first century. Priority issues relate to the lack of scientific understanding of lagoon functioning and variability, and include the need for reliable identification and classification of the resource, assessing responses to anthropogenic impacts (notably climate change) and applying ecosystem-specific management and

Handling editor: Pierluigi Viaroli N. A. Beer (&) C. B. Joyce School of Environment & Technology, University of Brighton, Cockroft Building, Lewes Road, Brighton BN2 4GJ, UK e-mail: [email protected]

monitoring. Key recommendations are (i) specialised surveys that recognise the inherent dynamism of the environment and facilitate a more accurate description of the lagoonal resource and its ecology, and (ii) an ecocomplex approach for conservation and management that addresses coastal habitat connectivity. Keywords Coastal lagoon Sea level rise Climate change Transitional waters Ecocomplex Ecosystem-based management

Introduction Coastal habitats are among the most important from both an ecological and a socio-economic perspective but are threatened by anthropogenic and climatic disturbance linked to rapid global population growth and land use alteration (Lotze et al., 2006; FitzGerald et al., 2008). Coastal lagoons are particularly important but especially vulnerable among coastal habitats (Gonenc & Wolflin, 2005). Defined as shallow coastal water bodies separated from the ocean by a barrier, connected at least intermittently to the ocean, lagoons are found on all continents and constitute 13% of global and 5% of European coastlines (Barnes, 1980; Kjerfve, 1994). Lagoons are ephemeral features in geological terms, typically lasting tens to hundreds of years. Natural ecological succession means lagoons are often anthrodependent, requiring periodic human intervention to maintain and conserve the lagoonal

123

2

Hydrobiologia (2013) 701:1–11

environment (Cognetti & Maltagliati, 2008). Coastal lagoons perform a range of ecosystem services of socio-economic value to coastal communities, including shoreline stabilisation, sediment and nutrient retention, high primary and secondary production, fisheries resources, habitat and food resources for terrestrial, aquatic and marine fauna, coastal water quality buffering, biomass and biodiversity reservation, and recreation and tourism amenities (Costanza et al., 1997; Gedan et al., 2011). Northern hemisphere lagoons are concentrated around the microtidal coastlines of the Mediterranean, Baltic and Black seas. North Atlantic lagoons are rare due to macrotidal range ([4 m) and natural habitat succession, and are unusual from a global viewpoint, often being confined by shingle rather than sand and frequently functionally connected to the sea via percolation rather than an inlet channel (Barnes, 1989). Five main physiographic sub-types have been described (Bamber et al., 1992; JNCC, 2007), each with its own sensitivities and threats (Table 1). As elsewhere, coastal population growth and development, land reclamation, coastal erosion, and the construction of sea defences have reduced the natural development of North Atlantic lagoons and caused the loss of many sites, as well as altering the delicate hydrological regime and community structure at remaining sites. Due to their vulnerability to climatic and anthropogenic disturbance, saline lagoons are listed as a priority habitat under

Annex I of the European Union Habitats Directive (EEC, 1992). The typically depauperate lagoonal community includes species almost or entirely restricted to lagoonal habitats—some to a single site—that represent some of Europe’s rarest plants and animals, consequently scheduled for statutory protection. However, generally little is known about the distribution and ecology of North Atlantic lagoonal ‘specialists’ as they are often small, cryptic and easily overlooked or misidentified, and mixohaline coastal habitats are generally under-surveyed, such that the lagoonal resource may be over-estimated (Joyce et al., 2005). Thus, the status of lagoonal specialists may be revised for at least some species as new data are collected, adding vital knowledge on the range and ecological requirements of under-recorded taxa (Gilliland & Sanderson, 2000). Two decades have passed since the last review of North Atlantic lagoons and the emergence of new threats, policies and challenges means that an updated assessment is now vital. In the context of increasing anthropogenic and climatic pressure on coastal resources, we summarise current ecological knowledge of North Atlantic lagoon systems and introduce contemporary issues, policies, concepts and techniques to identify the conservation, management and research challenges that need to be addressed if lagoons are to be safeguarded and sustainably managed in the twenty-first century.

Table 1 The five main physiographic sub-types of North Atlantic lagoon Isolated lagoons

Separated completely from the sea by a barrier of rock or sediment, isolated lagoons are especially transient features due to natural processes of infilling and coastal erosion. Seawater enters by limited ground water seepage or by over-topping of the barrier; salinity is variable but often low. Due to the limited water exchange the biota of isolated lagoons may be relatively impoverished

Percolation lagoons

Separated from the sea by shingle banks through which seawater percolates or occasionally over-tops. The water level shows some variation with tidal changes. Since percolation lagoons are normally formed by natural processes of sediment transport they may be eroded and swept away over a period of years or may become infilled by movement of the shingle bank

Silled lagoons

Water is retained at all states of the tide by a barrier of rock and tidal movement tends to be minimal. Seawater input is regular and frequent and although salinity may be seasonally variable it is usually high, except where the level of the sill is near to high tide level. Silled lagoons are restricted to the north and west of Scotland and may occur as sedimentary basins or in bedrock, where they are called obs

Sluiced lagoons

The natural movement of water between the lagoon and the sea has been modified by human mechanical interference such as the construction of culverts under a road or valved sluices. Communities may resemble those of silled lagoons but vary according to the substrate type and salinity

Lagoonal inlets

Ingressed on each tide and salinity is usually high, particularly at the seaward part of the inlet. Larger examples may have a number of different basins separated by sills, and demonstrate a complete gradient from full salinity through brackish to fresh water, significantly increasing habitat and species diversity

After Bamber et al. (1992) and JNCC (2007)

123


Summarising the research context Primary literature searches with the title keywords ‘coastal lagoon’, ‘saline lagoon’, ‘brackish lagoon’ and ‘barrier lagoon’ were conducted using ISI Web of Science (Thomson Reuters 2010). Studies included in our review investigate modern biological, ecological and physico-chemical phenomena in temperate coastal lagoon systems not only in the North Atlantic, but also the North Sea, Mediterranean, Adriatic, Aegean and Baltic in order to provide context. Studies focussing on coral reef lagoons were not included as these systems are morphologically and functionally distinct from higher latitude coastal barrier lagoons. Since 1975, 737 studies of northern hemisphere temperate coastal lagoon systems have been published as peer-reviewed journal and conference papers. Of these, 69% focussed on lagoon systems around microtidal Mediterranean, Adriatic and Baltic coastlines and 31% on macrotidal North Atlantic systems. The bias in research effort towards the more open Mediterranean and Adriatic lagoon systems reflects not just their relative abundance in this microtidal region, but also their extensive exploitation for fisheries and aquaculture, particularly of bivalve molluscs, and their proximity to major urban centres (for example, the Venetian Lagoon). It is evident that lagoons have rarely been compared between regions, probably because of structural and functional dissimilarities between micro and macrotidal ecosystems as well as different historical and cultural perspectives in southern and northern European lagoonal stakeholder communities. While there has been progress in our understanding of ecological functioning in European lagoons, especially in the Mediterranean and Baltic regions (e.g. Razinkovas et al., 2008), and the potential for climate change impacts upon European coastal lagoons is being investigated (e.g. Viaroli et al., 2007), knowledge of North Atlantic lagoon systems tends to lag behind other regions where interdisciplinary collaboration is well established (e.g. de Wit et al., 2012). A cited reference search was used to track progress in the understanding and conservation management of North Atlantic lagoons since the first calls for further research into their ecological functioning (Barnes, 1989, 1991a, b), which were mainly focussed upon the UK. These early papers highlighted a lack of recognition of the nature conservation importance of

3

lagoons and a limited knowledge of the factors that structure lagoonal communities, such that effective management was being constrained. A request for more integrated studies of lagoons was made (Barnes, 1991b) and initial implications for lagoons of sea level rise due to the ‘greenhouse effect’ were discussed. These papers have been cited by 19 studies that can be considered to directly advance our understanding of North Atlantic lagoonal communities and ecosystems, and their conservation and management challenges (Barnes, 1994a, 1999, 2005; Allen et al., 1995, Drake & Arias, 1997; Healy, 1997; Bamber, 1998; Barnes & Gandolfi, 1998; Gosling et al., 1998; Barnes & de Villiers, 2000; Small & Gosling, 2000; Porter et al., 2001; Ingolfsson, 2002; Greenwood & Wood, 2003; Foden et al., 2005; Joyce et al., 2005; Johnson et al., 2007; Pascual & Drake, 2008; Spencer & Brooks, 2012). Generally, these papers represent diverse studies addressing disparate research aims and individual species or sites ranging from southwest Spain via Great Britain and Ireland to Iceland, although concerted efforts were made to better understand the controls influencing the distribution and behaviour of some lagoonal taxa, such as Hydrobia (e.g. Barnes and Gandolfi, 1998; Barnes, 2005; Pascual & Drake, 2008). In addition, numerous lagoon surveys and site assessments have been published in the ‘grey literature’ by nature conservation agencies, especially since the 1990s in the UK where the information was collated in manuals to guide saline lagoon management and creation (e.g. Bamber et al., 2001). Recent publications have tended to continue to add to knowledge about the national or regional distribution of lagoonal taxa and their habitat, but research to date has failed to coalesce around the most significant issues affecting the ecosystem from an international perspective. Contemporary issues that affect North Atlantic coastal lagoons relate to the paucity of comparable scientific knowledge of lagoonal ecosystems and their landscape interactions, and increasingly include anthropogenic impacts such as climate change, coastal land use alteration and population growth. These are summarised in Fig. 1, which illustrates the critical role lagoons play linking terrestrial and marine systems, such that they may act as vital buffers and sensitive indicators to environmental change in coastal landscapes. Although anthropogenic effects are likely to increase, there are currently insufficient data to quantify

123

4


Fig. 1 A conceptual representation of the terrestrial and marine impacts on North Atlantic lagoons (left) and lagoonal influences on adjacent terrestrial and marine systems (right)

the threat they pose to lagoonal habitats and ecosystems (Barnes, 1992; JNCC, 2007), especially as the lagoonal resource itself, and the distribution and autecology of specialist species such as algae and invertebrates has not been accurately described for many taxa. Despite the efforts made in recent years to address the lack of understanding available to support sound management of North Atlantic lagoons, further research is needed to fill persistent knowledge gaps and meet emerging management challenges caused by anthropogenic impacts. Specific research that focusses on North Atlantic lagoons is merited in light of the environmental and biological dynamism that characterises the habitat, and is highly relevant under the EU Water and Marine Framework Directives and Integrated Coastal Zone Management (EEC, 2000, 2002, 2008) that provide a structure for integrated management of coastal waters (Mouillot et al., 2006; Basset, 2010). Research and management for North Atlantic lagoons should consider concepts such as ecosystembased management, and modern techniques such as stable isotope analysis, trace element analysis, biomonitoring and rapid biodiversity assessment techniques, some of which have recently been used effectively in lagoonal habitats elsewhere in Europe.

123

Challenges to management Concern has been expressed that the range of transitional and lagoon waters, which includes any partially saline surface water near the coast influenced by freshwater flows, is inadequately accounted for by current EU Directives (McLusky & Elliot, 2007; Bamber, 2010; Pe´rez-Ruzafa et al., 2011b), and a management strategy aimed specifically at coastal lagoons is required. Ecological understanding has not often to date been incorporated into effective management plans for individual North Atlantic lagoons; rather, management plans are usually based on limited data, often from estuarine systems that are unlikely to be directly comparable. Moreover, the distinct sensitivities of each physiographic lagoon type (Table 1) are not reflected by the current management framework, as understanding of the processes peculiar to each is currently inadequate to support such a tailored approach. High spatial variability in biotic and abiotic parameters within the lagoonal ecocomplex means that management plans might most effectively consider habitat patches individually (Benedetti-Cecchi et al., 2001).


A fundamental challenge to managers is the lack of a consistent approach to the classification of lagoonal habitats. Current estimates of the extent of lagoonal habitat around North Atlantic coastlines are likely to be exaggerated, for example by the inclusion of barbuilt estuaries. Surveys have shown that many coastal water bodies in southern England commonly assumed to be lagoons do not meet the hydrological and biological criteria for lagoon classification and are not of conservation significance as a lagoonal habitat (Joyce et al., 2005). Furthermore, some lagoons may not correspond to the definition of transitional waters given by the EU Water Framework Directive (EEC, 2000). Recognising that adjacent systems are closely linked is crucial for the effective understanding and management of coastal habitats, particularly for transitional zones that link terrestrial, freshwater and marine environments. Lagoons typically function as ecocomplexes, containing heterogeneous habitat networks and multiple linked ecosystems (e.g. wetland, intertidal sand/mud flat and pelagic systems). Many lagoons are incorporated within larger protected landscapes where the designation and management focusses upon other coastal habitats, such as salt marsh, mud flat or shingle beach, sometimes to the detriment of lagoon conservation. With the decline in environmental conditions widespread among lagoonal sites, attempts have been made to create artificial lagoons to replace or increase critical resources and habitat (Bamber et al., 1993); however, existing or newly created lagoons cannot be properly managed without understanding the fundamental ecological processes that occur and how these vary through time and space in response to environmental pressures. Attempts at habitat compensation should be planned in advance to allow sufficient time for the created habitats to become fully functional as lagoonal systems, rather than simply in reaction to accelerating habitat losses (Spencer & Brooks, 2012). Also, lagoonal plant and animal species have colonised human-created coastal water bodies, including gravel pits, marinas and docks (Allen et al., 1995; Joyce et al., 2005), but recognition of the value and the conservation of these ‘artificial’ sites tends to lag behind natural lagoons. While ecological degradation by non-native species may not yet be as apparent in North Atlantic lagoons as some freshwater aquatic and riparian systems, non-

5

native invertebrate fauna have been found in European coastal lagoons in recent years (e.g. Grabowski et al., 2006; Zaiko et al., 2007, 2009; Wozniczka et al., 2011) and represent a potential threat to lagoonal communities, possibly displacing native species and altering ecosystem functioning (Reise et al., 2006). Together with coastal inlets and embayments, coastal lagoons are considered ‘hot spots’ for alien invasions due to their steep environmental gradients, biological community structure and susceptibility to anthropogenic exploitation and pollution (Olenin & Leppa¨koski, 1999; Leppa¨koski et al., 2002; Paavola et al., 2005). Improving knowledge of North Atlantic lagoon ecosystems Joyce et al.’s (2005) study of the relationship between environmental and biological characteristics of 28 lagoons reinforced the critical role of the hydrological regime in structuring the community, but our understanding of dispersal and colonisation mechanisms has hardly progressed other than for a very few select species (Barnes, 1994b). While the distribution of marine and estuarine species within North Atlantic lagoons is likely to reflect their wider distribution in nearshore waters and hence their potential to colonise lagoons, the dispersal of lagoonal specialists is harder to explain. Invertebrate lagoonal specialists have at best minimally dispersive juvenile stages, and dispersal and colonisation at many sites may rely on the sporadic mass inflow of sea water as a source of biotic recruitment, perhaps facilitated by rafting on mats of filamentous algae (Barnes, 1988). Anthropogenic modification of connections between lagoon and adjacent marine systems could disrupt these processes, potentially interrupting immigration and rendering populations relict (Barnes, 1988). Although lagoon specialists can be persistent, the threat of population isolation and disappearance could be most severe among landlocked lagoons (Barnes, 1987). Occasional long-distance dispersal of the rare lagoonal specialist Nematostella vectensis, either by rafting events or by passive transport followed by asexual proliferation of populations, has resulted in the lack of genetic structure at large spatial scales within the UK (Pearson et al., 2002). Healy (1997) found no evidence for recolonisation of an Irish lagoon from adjacent brackish habitats, but observed rapid recolonisation by aquatic macroinvertebrates from peripheral refuges

123

6

following environmental fluctuations. As with other marine habitats, successful colonisation of coastal lagoons is likely to involve a large stochastic element (Barnes, 1987, 1988); added to the dynamic and unpredictable environment that characterises the habitat, the potential for recruitment presents considerable challenges to conservation management and research. In addition, unforeseen interspecific interactions with potentially stronger competitors can undermine efforts to conserve lagoonal specialists such as some molluscs (Barnes & Gandolfi, 1998). Lagoonal ecosystems can be both complex, with multiple organic matter sources, and dynamic, as environmental and hydrological fluctuations and eutrophication alter carbon routing through trophic levels. Connectivity between habitats within the lagoonal ecocomplex and between adjacent terrestrial, lagoonal and estuarine or open marine environments is also likely to be complex and variable, depending on lagoon morphology, climatic forcing and anthropogenic disturbance. Understanding this inherent complexity and dynamism necessitates a spatio-temporally explicit analytical approach but modern investigative techniques capable of resolving such issues are not commonly applied to North Atlantic lagoon systems, despite the availability of such techniques to researchers. Stable isotope analysis has been used to quantify the relative importance and trophic routing of terrestrial, marine and in situ primary production and nutrient recycling to Mediterranean lagoonal consumers (e.g. Vizzini & Mazzola, 2003, 2008; Vizzini et al., 2005) and to relate variability in food web structure to the degree of connectivity with adjacent environments and the level of anthropogenic disturbance (e.g. Carlier et al., 2008; Marin-Guirao et al., 2008). Carbon sources and trophic routing are likely to vary both within and between lagoons in response to hydrological regimes and ecotonal boundaries, meaning that assumptions drawn from Mediterranean studies may not be relevant to North Atlantic systems. The extent to which surplus macrophytic detritus, a major allochthonous carbon source in lagoonal food webs (Newell, 1982), is recycled by the microbial community can also influence basal food web structure (Danovaro & Pusceddu, 2007), but has not been considered in relation to North Atlantic lagoon ecosystems. The use of chemical analytical techniques to study ecological conditions in lagoonal waters and

123


sediments is difficult and expensive, as they require continuous monitoring of the highly changeable environmental variables; biomonitoring (e.g. monitoring benthic invertebrate assemblage and trait composition through time and space) provides effective information since it reflects the complex interaction between biotic and abiotic parameters (Debenay & Guillou, 2002). Studies seeking to explain North Atlantic lagoonal community structure in terms of physico-chemical environmental variables (e.g. Bamber et al., 1992; Joyce et al., 2005; Johnson et al., 2007) provide a useful starting point to develop biological and/or physical indicators of lagoon ecosystem health and functioning, but the success of an indicator approach relies on an appropriate sampling methodology and suite of taxa or ecological traits, that recognise multiple scales of spatial and temporal variability in the dynamic lagoon environment and community (Pe´rez-Ruzafa et al., 2007), especially given the stochastic nature of lagoon recruitment. One-off ‘snap-shot’ assessments of environmental and biological characteristics of a lagoon may misrepresent longer term conditions; for example a biological lag relative to environmental fluctuations means that recent saline intrusions may be evident in the community structure of a site that has reverted to freshwater conditions by the time of sampling, or vice versa (Healy, 1997; Joyce et al., 2005). In order to monitor and detect ecological changes to dynamic and threatened habitats such as lagoons, which are characterised by frequent and rapid fluctuations in abiotic conditions and communities with opportunistic or temporary species as well as permanent lagoon residents, an understanding is needed of baseline ecological processes and how these influence community-level dynamics. This is a central tenet of ecosystem-based management but the fundamental knowledge to underpin effective management of North Atlantic lagoon habitat is still limited, and efforts to manage existing habitats and create new habitat are compromised by this data deficiency. In such a highly dynamic and heterogeneous system, lagoonal biota are adapted to a high degree of natural environmental stress and ecological changes can be difficult to detect against the shifting baseline (Gamito et al., 2005), meaning that anthropogenic disturbances may not be apparent until the system is severely damaged (Elliott & Quintano, 2007; Pe´rez-Ruzafa et al., 2011a).


The use of in situ data loggers to record parameters such as temperature, salinity, chlorophyll and dissolved oxygen allows researchers to model the biological response to fine-scale spatial and temporal variability in the lagoonal environment (Falcao & Vale, 2003; Giardino et al., 2010). Remote sensing on the other hand allows broad spatial coverage and can provide useful insights into the longer term functioning of coastal habitats such as lagoons that can be difficult to monitor with traditional techniques (Flower & Thompson, 2009; Thompson & Flower, 2009; Giardino et al., 2010). A combination of these two approaches to facilitate full spatial coverage and continuous monitoring of key biotic and abiotic parameters in North Atlantic lagoons will be important to developing our understanding of these dynamic environments. Assessing and mitigating effects of anthropogenic changes Once an appreciation is gained of the scales at which natural dynamism is manifested in North Atlantic lagoonal ecosystems it may be feasible to develop a suite of biological indicators with the aim of quickly and efficiently detecting anthropogenic disturbances. Ecosystem functioning in Mediterranean lagoons is commonly investigated using invertebrate assemblage information (e.g. Lardicci & Rossi, 1998; Arvanitidis et al., 2005; Gamito & Furtado, 2009; Ponti et al., 2011), an approach that is also routinely used to assess and monitor freshwater environments, and could be employed to further our understanding of North Atlantic lagoonal ecosystem processes and functioning. Fish assemblages of North Atlantic lagoons have not been well characterised but the balance between transient and resident freshwater, brackish and marine communities could provide useful insights into the ecological status of a lagoon. For example, in the Mediterranean, ichthyofaunal diversity and structure indices have been developed as biological indicators of ecosystem functioning, anthropogenic disturbance, trophic structure and biomass, and nutrient export to adjacent marine and freshwaters (e.g. Mariani, 2001; Pe´rez-Ruzafa et al., 2006; Franco et al., 2009; Maci and Basset, 2009). Trace element analysis of Mediterranean and Adriatic lagoonal waters, sediments and biogenic carbonates has provided information on modern and

7

historical anthropogenic impacts (e.g. Martin et al., 1995; Guerra et al., 2007; Altun et al., 2009), biogeochemical cycling (e.g. Point et al., 2007; Pereira et al., 2009), nutrient limitation (e.g. Viaroli et al., 2005), the importance of lagoonal nursery areas for commercially important fish (e.g. Vasconcelos et al., 2008) and connectivity between adjacent environments (e.g. Abrantes et al., 2005). Trace elemental analysis could prove a powerful tool to elucidate connectivity among coastal habitats within lagoonal ecocomplexes and also to detect and monitor anthropogenic pollution in North Atlantic coastal water bodies. Conclusions: current status and research priorities Towards the end of the last century, concerns were voiced by Barnes (1989, 1991a, b) of gross managerial neglect of the rare and threatened North Atlantic lagoonal habitats and biota, stemming from a lack of awareness and scientific study. Since then, these lagoons have been more widely recognised for their conservation value and the managerial neglect has been at least partially redressed, but scientific understanding of the specific ecological and environmental processes that structure their communities is still limited. Other productive, mixohaline coastal habitats in the region, such as estuaries, have received considerably greater attention in the international literature whilst arguably being of a lower conservation importance. Saltmarsh habitats are threatened by coastal squeeze as lagoons are, but research effort to quantify the risks and model impacts far exceeds that for lagoons (e.g. Richards et al., 2008 and references therein). Given increasing concerns over climate change, including rising sea levels and increased storminess that will have major impacts on coastal lagoon ecosystems—particularly around macrotidal and storm-prone North Atlantic coastlines—further international, interdisciplinary research should be a high priority among coastal nations. This paper has identified that for North Atlantic lagoons such research should (i) aim to fill persistent knowledge gaps for lagoon ecosystems, (ii) develop more specific management and monitoring protocols and (iii) assess the effects of emerging anthropogenic impacts. The relationships between these priorities are indicated in Fig. 2, which also summarises the recommendations

123

8


Fig. 2 Schematic relationship between contemporary issues affecting North Atlantic coastal lagoons that require priority research action

discussed in this paper. Recommended actions include (i) targeted surveys and monitoring to determine the North Atlantic lagoon resource base more accurately and better establish its baseline ecology, (ii) a focus upon longer term, specialised methods that can characterise and assimilate the dynamic properties of the lagoonal environment, (iii) the development of a suite of biological indicators, such as fish and invertebrate taxa or traits, for lagoons and (iv) an ecocomplex approach that acknowledges the transitional and networked nature of lagoonal patches within the coastal landscape, enabling the use of techniques to elucidate habitat connectivity. Such research would facilitate more effective conservation of the North Atlantic lagoonal resource, including adaptive management in response to threats such as climate change and pollution. Acknowledgments This work was funded by the University of Brighton School of Environment and Technology Research Investment Fund. We thank G. Bilotta for his helpful comments on an earlier version of the manuscript.

References Abrantes, I., F. Rocha, J. Vidinha & J. A. Dias, 2005. Influence of Aveiro Lagoon heavy metal contents in the adjacent

123

continental shelf (Portugal). Ciencias Marinas 31(1B): 149–160. Allen, J. R., S. B. Wilkinson & S. J. Hawkins, 1995. Redeveloped docks as artificial lagoons: the development of brackish-water communities and potential for conservation of lagoonal species. Aquatic Conservation: Marine and Freshwater Ecosystems 5(4): 299–309. Altun, O., M. T. Sacan & A. K. Erdem, 2009. Water quality and heavy metal monitoring in water and sediment samples of the Ku¨c¸u¨kc¸ekmece Lagoon, Turkey (2002–2003). Environmental Monitoring and Assessment 151(1–4): 345–362. Arvanitidis, C., G. Chatzigeorgiou, D. Koutsoubas, T. Kevrekidis, C. Dounas, A. Eleftheriou, P. Koulouri & A. Mogias, 2005. Estimating lagoonal biodiversity in Greece: comparison of rapid assessment techniques. Helgoland Marine Research 59(3): 177–186. Bamber, R. N., 1998. Conservation of brackish lagoonal faunas. Journal of Conchology Suppl. 2: 265–269. Bamber, R. N., 2010. Coastal saline lagoons and the Water Framework Directive Natural England Commissioned Reports. Natural England, Peterborough. Bamber, R. N., S. D. Batten, M. Sheader & N. D. Bridgwater, 1992. On the ecology of brackish water lagoons in Great Britain. Aquatic Conservation: Marine and Freshwater Ecosystems 2(1): 65–94. Bamber, R. N., S. D. Batten & N. D. Bridgwater, 1993. Design criteria for the creation of brackish lagoons. Biodiversity and Conservation 2(2): 127–137. Bamber, R. N., P. M. Gilliland & M. E. A. Shardlow, 2001. Saline Lagoons: A Guide to Their Management and Creation. English Nature, Peterborough. Barnes, R. S. K., 1980. Coastal Lagoons. Cambridge University Press, Cambridge.

Hydrobiologia (2013) 701:1–11 Barnes, R. S. K., 1987. Coastal lagoons of East Anglia, UK. Journal of Coastal Research 3(4): 417–427. Barnes, R. S. K., 1988. The faunas of land-locked lagoons: chance differences and the problems of dispersal. Estuarine Coastal and Shelf Science 26(3): 309–318. Barnes, R. S. K., 1989. The coastal lagoons of Britain: an overview and conservation appraisal. Biological Conservation 49(4): 295–313. Barnes, R. S. K., 1991a. Dilemmas in the theory and practice of biological conservation as exemplified by British coastal lagoons. Biological Conservation 55(3): 315–328. Barnes, R. S. K., 1991b. European estuaries and lagoons: a personal overview of problems and possibilities for conservation and management. Aquatic Conservation: Marine and Freshwater Ecosystems 1(1): 79–87. Barnes, R. S. K., 1992. On the distribution of the northwest European species of the gastropod Hydrobia, with particular reference to H. neglecta. Journal of Conchology 34: 59–62. Barnes, R. S. K., 1994a. Investment in eggs in lagoonal Hydrobia ventrosa and life history strategies in north-west European Hydrobia species. Journal of the Marine Biological Association of the United Kingdom 74(3): 637–650. Barnes, R. S. K., 1994b. Macrofaunal community structure and life histories in coastal lagoons. In Kjerfve, B. (ed.), Coastal Lagoon Processes. Elsevier, Amsterdam: 311–362. Barnes, R. S. K., 1999. What determines the distribution of coastal hydrobiid mudsnails within north-western Europe? Marine Ecology: Pubblicazioni Della Stazione Zoologica Di Napoli I 20(2): 97–110. Barnes, R. S. K., 2005. Interspecific competition and rarity in mudsnails: feeding interactions between and within Hydrobia acuta neglecta and sympatric Hydrobia species. Aquatic Conservation: Marine and Freshwater Ecosystems 15(5): 485–493. Barnes, R. S. K. & C. J. de Villiers, 2000. Animal abundance and food availability in coastal lagoons and intertidal marine sediments. Journal of the Marine Biological Association of the United Kingdom 80(2): 193–202. Barnes, R. S. K. & S. M. Gandolfi, 1998. Is the lagoonal mudsnail Hydrobia neglecta rare because of competitively-induced reproductive depression and, if so, what are the implications for its conservation? Aquatic Conservation: Marine and Freshwater Ecosystems 8(6): 737–744. Basset, A., 2010. Aquatic science and the Water Framework Directive: a still open challenge towards ecogovernance of aquatic ecosystems. Aquatic Conservation: Marine and Freshwater Ecosystems 20(3): 245–249. Benedetti-Cecchi, L., F. Rindi, I. Bertocci, F. Bulleri & F. Cinelli, 2001. Spatial variation in development of epibenthic assemblages in a coastal lagoon. Estuarine Coastal and Shelf Science 52(5): 659–668. Carlier, A., P. Riera, J. M. Amouroux, J. Y. Bodiou, M. Desmalades & A. Gremare, 2008. Food web structure of two Mediterranean lagoons under varying degree of eutrophication. Journal of Sea Research 60(4): 287–298. Cognetti, G. & F. Maltagliati, 2008. Perspectives on the ecological assessment of transitional waters. Marine Pollution Bulletin 56: 607–608. Costanza, R., R. d’Arge, R. de Groot, S. Farber, M. Grasso, V. Hannon, K. Limburg, S. Naeem, R. V. O’Neill, J. Paruelo,

9 R. G. Raskin, P. Sutton & M. van den Belt, 1997. The value of the world’s ecosystem services and natural capital. Nature 287: 253–260. Danovaro, R. & A. Pusceddu, 2007. Biodiversity and ecosystem functioning in coastal lagoons: does microbial diversity play any role? Estuarine Coastal and Shelf Science 75(1–2): 4–12. de Wit, R., N. Mazouni & P. Viaroli, 2012. Research and management for the conservation of coastal lagoon ecosystems: South-North comparisons. Hydrobiologia. doi: 10.1007/s10750-012-1150-9. Debenay, J. P. & J. J. Guillou, 2002. Ecological transitions indicated by foraminiferal assemblages in paralic environments. Estuaries 25(6A): 1107–1120. Drake, P. & A. M. Arias, 1997. The effect of aquaculture practices on the benthic macroinvertebrate community of a lagoon system in the Bay of Cadiz (southwestern Spain). Estuaries 20(4): 677–688. EEC, 1992. Council Directive 92/43/EEC of 21 May 1992 on the Conservation of Natural Habitats and of Wild Fauna and Flora Official Journal of the European Communities, Series L, Vol. 206. EEC, Brussels: 7–50. EEC, 2000. Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for the Community action in the field of water policy Official Journal of the European Communities, Series L, Vol. 327. EEC, Brussels. EEC, 2002. Recommendation of the European Parliament and of the Council of 30 May 2002 concerning the implementation of Integrated Coastal Zone Management in Europe Official Journal of the European Communities, Series L, Vol. 148. EEC, Brussels: 24–27. EEC, 2008. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy Official Journal of the European Communities, Series L, Vol. 164. EEC, Brussels. Elliott, M. & V. Quintano, 2007. The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54: 640–645. Falcao, M. & C. Vale, 2003. Nutrient dynamics in a coastal lagoon (Ria Formosa, Portugal): the importance of lagoonsea water exchanges on the biological productivity. Ciencias Marinas 29(4): 425–433. FitzGerald, D. M., M. S. Fenster, B. A. Argow & I. V. Buynevich, 2008. Coastal impacts due to sea-level rise. Annual Review of Earth and Planetary Sciences 36: 601–647. Flower, R. J. & J. R. Thompson, 2009. An overview of integrated hydro-ecological studies in the MELMARINA Project: monitoring and modelling coastal lagoons-making management tools for aquatic resources in North Africa. Hydrobiologia 622: 3–14. Foden, J., D. A. Purdie, S. Morris & S. M. Nascimento, 2005. Epiphytic abundance and toxicity of Procentrum lima populations in the Fleet Lagoon, UK. Harmful Algae 4: 1063–1074. Franco, A., P. Torricelli & P. Franzoi, 2009. A habitat-specific fish-based approach to assess the ecological status of Mediterranean coastal lagoons. Marine Pollution Bulletin 58(11): 1704–1717.

123

10 Gamito, S. & R. Furtado, 2009. Feeding diversity in macroinvertebrate communities: a contribution to estimate the ecological status in shallow waters. Ecological Indicators 9(5): 1009–1019. Gamito, S., J. Gilabert, C. Marcos Diego & A. Pe´rez-Ruzafa, 2005. Effects of changing environmental conditions on lagoon ecology. In Gonenc, I. & J. Wolflin (eds), Coastal Lagoons: Ecosystem Processes and Modeling for Sustainable Use and Development. CRC Press, Boca Raton: 193–229. Gedan, K. B., M. L. Kirwan, E. Wolanski, E. B. Barbier & B. R. Silliman, 2011. The present and future role of coastal wetland vegetation in protecting shorelines: answering recent challenges to the paradigm. Climatic Change 106(1): 7–29. Giardino, C., M. Bresciani, R. Pilkaityte, M. Bartoli & A. Razinkovas, 2010. In situ measurements and satellite remote sensing of case 2 waters: first results from the Curonian Lagoon. Oceanologia 52(2): 197–210. Gilliland, P. M. & W. G. Sanderson, 2000. Re-evaluation of marine benthic species of nature conservation importance: a new perspective on certain ‘lagoonal specialists’ with particular emphasis on Alkmaria romijni Horst (Polychaeta : Ampharetidae). Aquatic Conservation: Marine and Freshwater Ecosystems 10(1): 1–12. Gonenc, I. E. & J. P. Wolflin, 2005. Coastal Lagoons: Ecosystem Processes and Modeling for Sustainable Use and Development. CRC Press, Boca Raton. Gosling, E. M., I. F. Wilson & J. Andrews, 1998. A preliminary study on genetic differentiation in Littorina saxatilis from Galway Bay, Ireland: Littorina tenebrosa Montagu—a valid species of ecotype? Hydrobiologia 378: 21–25. Grabowski, M., A. Konopacka, K. Jazdzewski & E. Janowska, 2006. Invasions of alien gammarid species and retreat of natives in the Vistula Lagoon (Baltic Sea, Poland). Helgoland Marine Research 60(2): 90–97. Greenwood, M. T. & P. J. Wood, 2003. Effects of seasonal variation in salinity on a population of Enochrus bicolor Fabricius 1792 (Coleoptera : Hydrophilidae) and implications for other beetles of conservation interest. Aquatic Conservation: Marine and Freshwater Ecosystems 13: 21–34. Guerra, R., A. Pasteris, M. Ponti, D. Fabbri & L. Bruzzi, 2007. Impact of dredging in a shallow coastal lagoon: Microtox (R) Basic Solid-Phase Test, trace metals and Corophium bioassay. Environment International 33(4): 469–473. Healy, B., 1997. Long-term changes in a brackish lagoon, Lady’s Island Lake, south-east Ireland. Biology and Environment: Proceedings of the Royal Irish Academy 97B(1): 33–51. Ingolfsson, A., 2002. The benthic macrofauna of coastal lagoons of Iceland: a survey in a sub-arctic macrotidal region. Sarsia 87(5): 378–391. JNCC, 2007. Second Report by the UK under Article 17 on the implementation of the Habitats Directive from January 2001 to December 2006. JNCC, Peterborough. Johnson, D. E., J. Bartlett & L. A. Nash, 2007. Coastal lagoon habitat re-creation potential in Hampshire, England. Marine Policy 31(5): 599–606. Joyce, C. B., C. Vina-Herbon & D. J. Metcalfe, 2005. Biotic variation in coastal water bodies in Sussex, England:

123

Hydrobiologia (2013) 701:1–11 implications for saline lagoons. Estuarine Coastal and Shelf Science 65(4): 633–644. Kjerfve, B., 1994. Coastal lagoon processes. In Kjerfve, B. (ed.), Coastal Lagoon Processes. Elsevier, Amsterdam: 1–8. Lardicci, C. & F. Rossi, 1998. Detection of stress on macrozoobenthos: evaluation of some methods in a coastal Mediterranean lagoon. Marine Environmental Research 45(4–5): 367–386. Leppa¨koski, E., S. Gollasch & S. Olenin, 2002. Invasive Aquatic Species of Europe: Distribution, Impacts and Management. Kluwer Academic Publishers, Dordrecht. Lotze, H. K., H. S. Lenihan, B. J. Bourque, R. H. Bradbury, R. G. Cooke, M. C. Kay, S. M. Kidwell, M. X. Kirby, C. H. Peterson & J. B. C. Jackson, 2006. Depletion, degradation and recovery potential of estuaries and coastal seas. Science 312: 1806–1809. Maci, S. & A. Basset, 2009. Composition, structural characteristics and temporal patterns of fish assemblages in nontidal Mediterranean lagoons: a case study. Estuarine Coastal and Shelf Science 83(4): 602–612. Mariani, S., 2001. Can spatial distribution of ichthyofauna describe marine influence on coastal lagoons? A central Mediterranean case study. Estuarine Coastal and Shelf Science 52(2): 261–267. Marin-Guirao, L., J. Lloret & A. Marin, 2008. Carbon and nitrogen stable isotopes and metal concentration in food webs from a mining-impacted coastal lagoon. Science of the Total Environment 393(1): 118–130. Martin, J. M., M. H. Dai & G. Cauwet, 1995. Significance of colloids in the biogeochemical cycling of organic carbon and trace metals in the Venice Lagoon (Italy). Limnology and Oceanography 40(1): 119–131. McLusky, D. S. & M. Elliot, 2007. Transitional waters: a new approach, semantics or just muddying the waters? Estuarine, Coastal and Shelf Science 71: 359–363. Mouillot, D., S. Spatharis, S. Reizopoulou, T. Laugier, L. Sabetta, A. Basset & T. D. Chi, 2006. Alternatives to taxonomic-based approaches to assess changes in transitional water communities. Aquatic Conservation: Marine and Freshwater Ecosystems 16(5): 469–482. Newell, R. C., 1982. The energetics of detritus utilisation in coastal lagoons and nearshore waters. Oceanologica Acta 5: 347–355. Olenin, S. & E. Leppa¨koski, 1999. Non-native animals in the Baltic Sea: alteration of benthic habitats in coastal inlets and lagoons. Hydrobiologia 393: 233–243. Paavola, M., S. Olenin & E. Leppa¨koski, 2005. Are invasive species most successful in habitats of low native species richness across European brackish water seas? Estuarine, Coastal and Shelf Science 64(4): 738–750. Pascual, E. & P. Drake, 2008. Physiological and behavioral responses of the mud snails Hydrobia glyca and Hydrobia ulvae to extreme water temperatures and salinities: implications for their spatial distribution within a system of temperate lagoons. Physiological and Biochemical Zoology 81(5): 594–604. Pearson, C. V. M., A. D. Rogers & M. Sheader, 2002. The genetic structure of the rare lagoonal sea anemone, Nematostella vectensis Stephenson (Cnidaria; Anthozoa) in the United Kingdom based on RAPD analysis. Molecular Ecology 11: 2285–2293.

Hydrobiologia (2013) 701:1–11 Pereira, E., M. Otero, P. Monterroso, C. Vale & A. C. Duarte, 2009. Transport of trace metals (Cd, Pb and Cu) in a coastal temperate lagoon. Fresenius Environmental Bulletin 18(1): 70–81. Pe´rez-Ruzafa, A., J. A. Garcia-Charton, E. Barcala & C. Marcos, 2006. Changes in benthic fish assemblages as a consequence of coastal works in a coastal lagoon: the Mar Menor (Spain, Western Mediterranean). Marine Pollution Bulletin 53(1–4): 107–120. Pe´rez-Ruzafa, A., C. Marcos, I. M. Pe´rez-Ruzafa, E. Barcala, M. I. Hegazi & J. Quispe, 2007. Detecting changes resulting from human pressure in a naturally quick-changing and heterogeneous environment: spatial and temporal scales of variability in coastal lagoons. Estuarine Coastal and Shelf Science 75(1–2): 175–188. Pe´rez-Ruzafa, A., C. Marcos & I. M. Pe´rez-Ruzafa, 2011a. Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Physics and Chemistry of the Earth 36(5–6): 160–166. Pe´rez-Ruzafa, A., C. Marcos, I. M. Pe´rez-Ruzafa & M. Pe´rezMarcos, 2011b. Coastal lagoons: ‘‘transitional ecosystems’’ between transitional and coastal waters. Journal of Coastal Conservation 15(3): 369–392. Point, D., M. Monperrus, E. Tessier, D. Amouroux, L. Chauvaud, G. Thouzeau, F. Jean, E. Amice, J. Grall, A. Leynaert, J. Clavier & O. F. X. Donard, 2007. Biological control of trace metal and organometal benthic fluxes in a eutrophic lagoon (Thau Lagoon, Mediterranean Sea, France). Estuarine Coastal and Shelf Science 72(3): 457–471. Ponti, M., C. Casselli & M. Abbiati, 2011. Anthropogenic disturbance and spatial heterogeneity of macrobenthic invertebrate assemblages in coastal lagoons: the study case of Pialassa Baiona (northern Adriatic Sea). Helgoland Marine Research 65(1): 25–42. Porter, J. S., P. E. J. Dyrynda, J. S. Ryland & G. R. Carvalho, 2001. Morphological and genetic adaptation to a lagoon environment: a case study in the bryozoan genus Alcyonidium. Marine Biology 139(3): 575–585. Razinkovas, A., Z. Gasiu¯nait_e, J. M. Zaldivar & P. Viaroli, 2008. European lagoons and their watersheds: function and biodiversity. Hydrobiologia 611: 1–179. Reise, K., S. Olenin & D. Thieltges, 2006. Are aliens threatening European aquatic coastal ecosystems? Helgoland Marine Research 60(2): 77–83. Richards, J. A., M. Mokrech, P. M. Berry & R. J. Nicholls, 2008. Regional assessment of climate change impacts on coastal and fluvial ecosystems and the scope for adaptation. Climatic Change 90(1–2): 141–167.

11 Small, M. P. & E. M. Gosling, 2000. Species relationships and population structure of Littorina saxatilis Olivi and L. tenebrosa Montagu in Ireland using single-strand conformational polymorphisms (SSCPs) of cytochrome b fragments. Molecular Ecology 9(1): 39–52. Spencer, T. & S. M. Brooks, 2012. Methodologies for measuring and modelling change in coastal saline lagoons under historic and accelerated sea-level rise, Suffolk coast, eastern England. Hydrobiologia 693(1): 99–115. Thompson, J. R. & R. J. Flower, 2009. Environmental science and management of coastal lagoons in the Southern Mediterranean Region: key issues revealed by the MELMARINA Project. Hydrobiologia 622: 221–232. Vasconcelos, R. P., P. Reis-Santos, S. Tanner, A. Maia, C. Latkoczy, D. Gunther, M. J. Costa & H. Cabral, 2008. Evidence of estuarine nursery origin of five coastal fish species along the Portuguese coast through otolith elemental fingerprints. Estuarine Coastal and Shelf Science 79(2): 317–327. Viaroli, P., M. Bartoli, R. Azzoni, G. Giordani, C. Mucchino, M. Naldi, D. Nizzoli & L. Taje, 2005. Nutrient and iron limitation to Ulva blooms in a eutrophic coastal lagoon (Sacca di Goro, Italy). Hydrobiologia 550: 57–71. Viaroli, P., P. Lasserre & P. Campostrini, 2007. Lagoons and coastal wetlands in the global change context: impacts and management issues. Hydrobiologia 577: 1–168. Vizzini, S. & A. Mazzola, 2003. Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Marine Biology 142(5): 1009–1018. Vizzini, S. & A. Mazzola, 2008. The fate of organic matter sources in coastal environments: a comparison of three Mediterranean lagoons. Hydrobiologia 611: 67–79. Vizzini, S., B. Savona, T. D. Chi & A. Mazzola, 2005. Spatial variability of stable carbon and nitrogen isotope ratios in a Mediterranean coastal lagoon. Hydrobiologia 550: 73–82. Wozniczka, A., S. Gromisz & N. Wolnomiejski, 2011. Hypania invalida (Grube, 1960), a polychaete species new for the southern Baltic estuarine area: the Szczecin Lagoon and the River Odra mouth. Aquatic Invasions 6(1): 39–46. Zaiko, A., S. Olenin, D. Daunys & T. Nalepa, 2007. Vulnerability of benthic habitats to the aquatic invasive species. Biological Invasions 9(6): 703–714. Zaiko, A., D. Daunys & S. Olenin, 2009. Habitat engineering by the invasive zebra mussel Dreissena polymorpha (Pallas) in a boreal coastal lagoon: impact on biodiversity. Helgoland Marine Research 63(1): 85–94.

123