Climate change and loss of saltmarshes - Wiley Online Library

Ibis (2004), 146 (Suppl.1), 21– 28

Blackwell Publishing, Ltd.

Climate change and loss of saltmarshes: consequences for birds

R. G. HUGHES* School of Biological Sciences, Queen Mary and Westfield College, University of London, London E1 4NS, UK

Saltmarshes are areas of vegetation subject to tidal inundation and are important to birds for several reasons. Saltmarshes are areas of high primary productivity and their greatest significance for coastal birds is probably as the base of estuarine food webs, because saltmarshes export considerable amounts of organic carbon to adjacent habitats, particularly to the invertebrates of mudflats. In addition, saltmarshes are of direct importance to birds by providing sites for feeding, nesting and roosting. Climate change can affect saltmarshes in a number of ways, including through sea-level rise. When sea-level rises the marsh vegetation moves upward and inland but sea walls that prevent this are said to lead to coastal squeeze and loss of marsh area. However, evidence from southeast England, and elsewhere, indicates that sea-level rise does not necessarily lead to loss of marsh area because marshes accrete vertically and maintain their elevation with respect to sea-level where the supply of sediment is sufficient. Organogenic marshes and those in areas where sediment may be more limiting (e.g. some west coast areas) may be more susceptible to coastal squeeze, as may other marshes, if some extreme predictions of accelerated rates of sea-level rise are realized.

SALTMARSHES: DEVELOPMENT, CHARACTERISTICS AND IMPORTANCE Saltmarshes are areas of vegetation on temperate wave-sheltered shores, usually between mean high water neap tide level (MHWNTL) and mean high water spring tide level (MHWSTL). The usual explanation of the development of saltmarsh is by facilitated succession, whereby plants relatively tolerant of the conditions associated with immersion by sea-water first colonize bare sediment. These plants, which include microphytobenthos, particularly epipelic diatoms, filamentous algae and vascular plants such as Zostera spp., enhance sediment accretion and stability leading to an increase in its elevation. The elevated sediment becomes suitable for colonization by pioneer zone saltmarsh plant species, such as Salicornia europaea, Suaeda maritima and Spartina anglica, that are less able to cope with prolonged inundation by sea-water. These plants, in turn, promote further sediment accretion, facilitating colonization by low to midmarsh species, such as Puccinellia maritima and Atriplex portulacoides. The outcome of *Email: [email protected]

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these processes may be zonation (Fig. 1), where each plant species occurs in a zone, the lower limit of which is determined by their tolerance to inundation by sea-water and the upper limit by biological interactions, particularly interspecific competition with plant species less able to tolerate inundation by seawater. However, as the marsh develops, subsequent sediment deposition and accretion will tend to occur at the seaward edge, where the sediment supply is greatest and first intercepted by the plants. The once sloping marsh progressively becomes flatter and where a saltmarsh is approximately horizontal the vegetation may be of relatively low diversity, being dominated by a few species best suited to the particular height of the marsh surface. For example, at Tollesbury, Essex (Fig. 2), the approximately flat marsh surface is dominated by Puccinellia and Atriplex (Garbutt et al. 2000), the latter being particularly common at the edges of the tidal creeks that dissect the marsh. Salicornia and Suaeda dominate the sparse vegetation of the pioneer zone, mostly in the tidal creeks. It is becoming increasingly apparent that an observed zonation of vegetation may not be the product of a recent ecological succession (see Davy 2000 for a review). The vegetation zones may have been in their current locations for centuries if there

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Figure 1. Profile diagram of a typical northwest European saltmarsh, illustrating the relative positions of some of the most abundant species (modified from Burd 1992).

Figure 2. Part of the saltmarsh at Tollesbury, Essex, showing the approximately flat marsh surface excised by an extensive creek network.

has been little sediment accretion, and indeed even if there has been a great deal. Funnell and Pearson (1989) took 30 deep cores in various substrata along the north Norfolk coast, 23 of which were in upper saltmarsh habitats. Of these, only seven were underlain by lower marsh vegetation, indicating upper marsh development need not be preceded by facilitated succession from lower marsh communities. The depth of upper marsh vegetation in their cores varied up to 6–9 m in their eastern sites (Stiffkey, Morston and Cley), indicating that the basic morphology of the marsh may have been established several thousand years ago. Thus, for example, the morphology of the Tollesbury marsh (Fig. 3) can be interpreted in two ways. The creeks may be erosional features, where the once more extensive marsh surface has been excised by tidal currents to form creeks that progressively become wider and deeper. Under this interpretation up to approximately half of the vegetated surface may have been lost. Some lateral erosion of the creeks is apparent (Paramor & Hughes 2004) but this erosion, like that of the marshes in general, may be relatively recent (see below). Alternatively,

© 2004 British Ornithologists’ Union, Ibis, 146 (Suppl.1), 21–28

Figure 3. Aerial photograph of part of the Tollesbury saltmarsh (and to the right part of the Tollesbury managed realignment site), illustrating the extent of the creek network and the presence of deep basins close to the sea walls (bottom left). Note that approximately half of the marsh area is unvegetated.

the basic creek pattern could have been established a long time ago and the vegetated areas between the creeks have accreted sediment, under conditions of isostatic sea-level rise, leading to the deepening of the creeks. A recent study has shown that the marsh surface is accreting sediment at a rate at least equal to isostatic sea-level rise (Cahoon et al. 2000). Under this interpretation, little vegetation has been lost by erosion. Thus without an appreciation of the ecological history of a marsh it becomes difficult to interpret how climate change and sea-level rise will affect it. Saltmarshes are areas of high primary productivity. For example, the productivity of both Puccinellia and Spartina were estimated to be approximately 1400 g/m2/ yr (Long & Mason 1983), similar to values

Consequences of climate change and saltmarsh loss on birds

for tropical rainforest and temperate grasslands. One of the major effects of saltmarshes in estuaries is the creation of organic matter that fuels detritus-based food webs in the marsh, and through export to adjacent habitats (Teal & Howes 2000, Valiela et al. 2000). Valiela et al. (2000) reviewed the evidence for export from, or import to, saltmarshes and concluded that in general mature marshes exported organic carbon whereas young marshes, dominated by pioneer zone vegetation, tended to be net importers. Much of the exported organic material is as detritus (particulate organic carbon – POC) or dissolved organic carbon (DOC), which, directly or indirectly, sustains invertebrates of the mudflats and deeper waters, and then birds and fish. The primary productivity of benthic microphytobenthos in vegetated saltmarshes can also be high (28–341 g/m2/ yr) (Sullivan & Currin 2000) and may be a major component of saltmarsh food webs as they are more readily consumed by a range of invertebrates. The range of productivity estimates of microphytobenthos on mudflats is somewhat lower (29–234 g/m2/yr) (Underwood & Kromkamp 1999), and in general mudflats are net consumers of organic material through microbial decomposition and consumption by deposit-feeding invertebrates. The relative importance of the different sources of organic carbon in an estuary (primary productivity of marsh, mudflat and phytoplankton, and the export–import balance to and from the river and sea) will be site specific and depend largely on the extent of each habitat type, flows, tidal volume and turbidity of the water. Despite these uncertainties, saltmarshes are regarded as important areas for primary productivity, especially in small estuaries where they form a relatively large proportion of the intertidal area. USE OF SALTMARSHES BY BIRDS Saltmarshes are important for birds directly, as feeding, roosting and nesting sites, and indirectly, mainly through their position at the base of estuarine food webs. Waders tend not to feed in saltmarshes to any great extent, as invertebrates are less abundant in vegetated areas than in open mudflats, but Common Redshank Tringa totanus and, in particular, Common Snipe Gallinago gallinago may feed in the creeks and salt pans on marshes (Ferns 1992). Where Spartina, for example, spreads across mudflats the feeding opportunities to waders (e.g. Dunlin Calidris alpina) decline and this may be important as these mudflats are at the top of the beach that is exposed by the tide

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for the longest time (Davis & Moss 1984, Goss-Custard & Moser 1988) and some extreme remedies for removing spreading vegetation have been attempted (Frid et al. 1999). The seeds of saltmarsh plants are eaten by a variety of birds, including passerines that feed on the small seeds of Salicornia and Suaeda in winter (Brown & Atkinson 1996), and a range of duck species including Eurasian Teal Anas crecca, Mallard A. platyrhynchos and Northern Pintail A. acuta. Saltmarsh vegetation is consumed by relatively few bird species. Geese, including Brent Geese Branta bernicla, and Eurasian Wigeon A. penelope consume Puccinellia (saltmarsh grass) preferentially (Rowcliffe et al. 1995) but their diet when on an estuary is often dominated by Zostera (eelgrass) and filamentous green algae that contain less indigestible cellulose and more protein. Brent Geese may be particularly dependent on saltmarshes late in the winter as they tend to feed on Zostera early in the winter, then Enteromorpha and then short saltmarsh plants (mostly Puccinellia) from January onward (Charman & Macey 1978). The relative lack of disturbance to birds on saltmarshes may explain why some birds feed there in preference to nearby fields where higher quality food (e.g. autumn sown cereals) is available (Ferns 1992). Saltmarshes may be important roosting and nesting areas for many bird species as these areas are relatively undisturbed and close to their feeding areas. Ferns (1992) lists some of the many waders, wildfowl, gulls, passerines and other species that nest in saltmarshes. All saltmarsh vegetation is inundated by the highest spring tides that occur around the spring and autumn equinoxes, but in summer (May to August) the highest areas may not be reached by the spring tides and may be a convenient and relatively undisturbed nesting area. Saltmarshes are particularly important to Common Redshank and 60% of the British population nests there. Common Redshank eggs can survive some inundation by sea-water if incubation is resumed soon after the tide has ebbed. Saltmarshes may also benefit birds indirectly by absorbing wave energy, and reducing erosion, run-up and over-topping of any sea walls, and they may protect from saltwater intrusion adjacent habitats of high value to birds, such as freshwater marshes and grazing marshes. EFFECTS OF GLOBAL WARMING ON SALTMARSHES The properties of saltmarshes generally depend on the specific composition of the vegetation, and factors

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that affect the vegetation community of a marsh can affect the value of the marsh to birds and to the bioeconomy of the estuarine system. There is much still not known about the ecology of saltmarshes, the biology of the plant and animal species, and estuarine ecosystems in general, and consequently conclusions about the potential effects of global warming on saltmarshes must be speculative. Global warming can affect saltmarshes in two broad ways, through change in the climate and by sea-level rise. Climate change Bertness and Pennings (2000) argued that the zonation of saltmarsh plants might be influenced by nutrient enrichment (eutrophication) and by climate. Climate (temperature) affects the rates of biological and chemical processes in saltmarshes, including photosynthesis, transpiration, decomposition, nutrient cycling and the accumulation or organic matter, all of which, together with the direct effect of temperature, may affect plant distributions. Bertness and Pennings (2000) suggested that climate plays a major role in saltmarsh community structure by changing soil salinity. Climate change may increase the rate of evaporation on the soil surface and hence increase salt concentration, or by increasing the rate of precipitation reduce the salinity of the soil. High salinities are usually found at mid marsh elevations, because lower soils are more frequently flushed by the tide and higher elevations are dominated more by rain and less by tidal inundation. High soil salinities may lead to the death of plants and the formation of salt pans, areas of bare mud that may, or may not, retain water. In both cases the habitat is unsuitable for further colonization because the salinity remains high and the pans remain or increase in size as these areas of unprotected sediment are more susceptible to physical erosion than the surrounding vegetated marsh. Salt pans may be colonized by invertebrates usually associated with the mudflats and provide sheltered feeding areas for waders such as Common Snipe. The productivity of marine plants is generally nitrogen limited (Valiela 1984), and addition of nitrogen, through eutrophication or by increased precipitation caused by climate change, can increase the productivity of a marsh and increase the food value of plants to herbivores (Teal & Howes 2000). Increased precipitation, one forecast effect of climate change, may increase the supply of sediment brought to the marsh by rivers and increase the rate of accretion of


the marsh surface, allowing the marsh surface to keep pace with accelerating sea-level rise (see below). Increased precipitation, which lessens the feeding efficiency of sight-feeders, such as plovers, by disturbing the sediment surface, may reduce invertebrate mortality rates and lead to an increase in herbivory/ bioturbation. Daborn et al. (1993) described a trophic cascade, in which predation by the Semipalmated Sandpiper Calidris pusilla on Corophium volutator was responsible for an increase in sediment stability by allowing microphytobenthos (otherwise consumed by Corophium) to proliferate. Herbivory and bioturbation by invertebrates, particularly the ragworm Nereis diversicolor, are responsible for some of the extensive loss of marshes in southeast England (Hughes 2001, Paramor & Hughes 2004). Increased temperatures could also increase the activity of invertebrates and by changing their abundances and distributions could affect the rate of herbivory and bioturbation, contributing further to the loss of some saltmarshes (see below). Sea-level rise One response of saltmarshes to sea-level rise is a landward migration, such that the vegetation zonation is maintained relative to sea-level. If this upward progression is prevented by the presence of sea walls the marsh is said to be squeezed, and ultimately could disappear. As sea-level rises the lower limits to the potential niche of each plant species moves upward and the expectation is that the upper species will disappear first and the pioneer zone species, those most able to cope with inundation, will disappear last. However, this progressive loss of species will not necessarily occur at a rate proportional to the rate of rise in sea-level. For example, in a mature flat marsh dominated by Puccinellia, such as at Tollesbury, a small rise in sea-level across the critical threshold of the lower limit of its potential niche would cause much of the marsh vegetation to revert to one dominated by pioneer zone species. This would be detrimental to birds as the short saltmarsh grass preferred by geese and Eurasian Wigeon would be replaced by less palatable, and less productive, pioneer zone species. Coastal squeeze will reduce the total area of saltmarsh, reduce primary productivity and reduce the time that is available to birds for feeding, roosting and nesting. For example, Brent Geese are relatively small and need to feed for a greater proportion of the time than larger geese. Consequently, they depend


more than other species on the higher saltmarsh vegetation that is available for more of each tidal cycle. Brent Geese need to feed at night, particularly following warm days when a larger proportion of the day was spent in non-feeding activities, and on cold nights (Lane & Hassall 1996). Thus increasing temperatures associated with climate change could cause the birds to change their behaviour to depend to a greater extent on the marsh vegetation that could be available for less time because of sea-level rise. Successful rearing of young from nests on saltmarshes will decline as progressively less of the available vegetation will remain above the spring tides in the summer months. Birds are capable of moving large quantities of nutrients from their feeding grounds, mudflats and terrestrial sites, to their roosting sites. Post et al. (1998) estimated that geese were responsible for 40% and 75% of the imported nitrogen and phosphorous, respectively, into a freshwater wetland. The significance of the defecation of roosting waders and wildfowl on nutrient enrichment of saltmarsh vegetation is likely to be less than this freshwater example, but a decline in primary productivity from this source is one potential consequence of coastal squeeze. There could also be more subtle but important consequences for the ecology of the marsh and the surrounding estuary, as plant species within saltmarshes have different properties, including primary productivity, ability to accrete and bind sediment, and their effects on nutrient cycling. In general, primary productivity in marine and estuarine ecosystems, including saltmarshes, is nitrogen limited (see above), and one of the important ecosystem processes that occurs within saltmarshes is nitrogen cycling. Thomas and Christian (2001) compared the ability of different plant communities within a saltmarsh to cycle nitrogen in the context of rising sea-levels. They concluded that under coastal squeeze, not only will there be a reduction in total marsh area, but the marsh will cycle less nitrogen per unit area because the high marsh will decrease in size relative to the low marsh. Sea-level rise may reduce the intertidal area of mudflat within an estuary, especially in an estuary constrained by sea walls. However, mudflat area per se may be unimportant for birds. What is important is the biomass and availability of invertebrate food, which depend ultimately on primary productivity elsewhere, and the time the mudflat is exposed by the tide and available to birds. Thus sea-level rise

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could carry a double problem for waders, a reduction in saltmarsh productivity and a decline in the time their potential food is available. The outcome is a reduction in the carrying capacity of the estuary for birds. One potential consequence of sea-level rise is the construction of sea walls behind saltmarshes where currently they do not exist. This could lead to several long-term consequences, including those associated with coastal squeeze, and they may lead to changes in the abundance and distribution of plants. Sea walls reflect wave energy back onto the marsh, increasing the physical erosion of the vegetation, and this perhaps together with an increase in the formation of erodable salt pans may be one reason why many marshes of southeast England are characterized by the presence of deep basins close to the sea walls (Fig. 3). Sea walls separate saltmarshes from the adjacent terrestrial habitats and one consequence of this is the lack of runoff or percolation of groundwater. This water is of relatively low salinity, which may have led to an increase in salinity of the upper and mid marsh soils, thereby contributing to the formation of salt pans (see above). Where saltmarshes are still in contact with terrestrial communities they may intercept nitrogen in the groundwater (especially in fertilized arable areas), increasing productivity and acting as a buffer between the land and the estuary. Thus these saltmarshes may have a beneficial effect on, for example, intertidal eelgrasses (Zostera spp.), which are affected negatively by enriched nitrogen concentrations (Touchette & Burkholder 2000, Valiela et al. 2000). In the agricultural estuaries of southeast England the sea walls may have reduced this buffering capacity, as groundwater usually collects in borrow dykes inside the sea walls and flows to the estuary through sluices protected on their seaward side by simple flap-valves. This flow occurs mostly on the ebbing tide and the nutrients do not reach the marsh vegetation immediately, if at all, and when they do, on subsequent rising tides, they will be much diluted. Instead, the water flows onto the mudflats where its nutrients may continue to contribute to the demise of eelgrasses, with concomitant effects on system productivity, sediment stability and direct effects on herbivorous birds such as Brent Geese and Eurasian Wigeon. However, nutrient enrichment may promote the growth of opportunistic green algae on the mud/ sandflats (see Raffaelli 1999 for a review). The growth of these algae may also be promoted by climate change, as indicated by the fact that in the Ythan


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Estuary of northeast Scotland macroalgal blooms were correlated with higher spring temperatures (Raffaelli 1999). Although these algae increase system productivity and are consumed by herbivorous birds, algal mats have negative effects on mudflat invertebrates, particularly Corophium, a common prey item of waders and fish. When algal mats were common, the food intake of Common Redshank, Bar-tailed Godwit Limosa lapponica and Eurasian Curlew Numenius arquata declined ( Raffaelli 1999). SEA-LEVEL RISE AND SALTMARS HES OF SOUTHEAST ENGLAND One way to predict the effects of eustatic sea-level rise (caused by global warming) on saltmarshes is to examine saltmarshes in areas that have experienced sea-level rise already. The extensive and continuing loss of marshes in southeast England (40 ha/yr) has been attributed to coastal squeeze, as these coasts have experienced sea-level rise for several thousand years, because of isostatic rebound following the retreat of the glaciers that covered northern Britain. However, in that time extensive saltmarshes have developed; for example, the ports of Cley-next-theSea in Norfolk and Rye in East Sussex are now separated from the sea by over 1 km of (reclaimed) marsh. Approximately 40 000 ha of saltmarsh developed in the Essex estuaries but only about 10% remains (Dixon et al. 1998), largely because of the successive reclamations that have occurred since medieval times, and some erosion over the past 50 years. There is therefore no rational basis for believing that sea-level rise will inevitably lead to loss of saltmarsh through coastal squeeze. Hughes and Paramor (2004) present several arguments against coastal squeeze as the explanation for marsh erosion in southeast England, paramount among which is the fact that when sealevel rises saltmarshes accrete vertically and keep pace with sea-level rise. The surface of the sediment, vegetated or bare sediment, relative to sea-level varies in dynamic equilibrium between sediment deposition and resuspension according to local physical and biological conditions (e.g. Hughes 2001). Sea-level rise should lead to an accelerated rate of sedimentation, if the sediment supply is sufficient, because more sedimentladen water flows over the vegetated marsh, the water is deeper and the residence time is longer. The expectation is that as sea-level rises the marsh surface should accrete and maintain its dynamic equilibrium


elevation relative to sea-level. Indeed, in some Essex marshes the rates of accretion have led to rates of elevation changes estimated to be at least as high as the presumed 1.5 mm/yr isostatic rise in sea-level in the short term (Cahoon et al. 2000) and on a decadal scale (Pye 2000). There is evidence that this relationship has also held in the longer term (see Davy 2000 for a review). The height of existing marshes above the level of reclaimed marshes indicates long-term (centuries) accretion rates of about 1.5 mm/yr, and palaeoecolgical evidence from the north Norfolk coast indicates similar sea-level rises over several millennia. The depth (up to 9 m) of upper marsh vegetation in the cores taken by Funnell and Pearson (1989) from some Norfolk saltmarshes indicates that the elevation of the marshes (and the potential niches of the plant species) has kept pace with this isostatic sea-level rise for several millennia. So, far from explaining the loss of marshes, sea-level rise has been important in the development of saltmarshes of southeast England that has allowed the successive reclamations that have taken place over centuries in some estuaries. Sea walls will prevent the landward movement of marshes, but not their vertical development, and sea walls cannot explain loss of marshes; they only restrict the increase in area with sea-level rise. However, whether sediment accretion and the success of saltmarsh vegetation can be maintained under more rapid sea-level rise, and current predictions being used by the Environment Agency are up to 6 mm/yr, remains to be seen (Hughes & Paramor 2004). The balance between deposition and resuspension of sediment may be shifted by other elements of climate change, for example increased wave action and tidal currents, and increased precipitation leading to more sediment being brought to the estuaries by rivers. The marshes under most threat from sea-level rise may be those where the sediment supply may be insufficient. These include the organogenic marshes of the USA and some on the west coast of the UK where the sea-water is less turbid than the North Sea and the rivers drain harder rocks and contain less sediment. Loss of saltmarsh vegetation in southeast England can be attributed to herbivory and bioturbation by the invertebrate macrofauna, especially the ragworm Nereis diversicolor (Hughes 1998, 2001, Hughes et al. 2000, Paramor & Hughes 2004). In experiments in which surface deposit feeding by Nereis diversicolor was prevented, the community was switched from an invertebrate-dominated eroding


mud to plant-dominated accreting mud. Creek erosion is exacerbated by invertebrates and possibly by increased tidal current speeds caused by an increase in the tidal range of the southern North Sea (Pye 2000). This creek erosion entrains a positive feedback whereby the erosive potential of the tidal currents that flow through the creek system increases due to the enlarged volume that flows on each tide. The interactions of plants and invertebrates at the saltmarsh–mudflat interface are clearly important, as are the factors that affect the rates of these processes. How these will change in a future affected by global warming and climate change will be particularly important where invertebrates are limiting the abundance and distribution of saltmarsh plants. REFERENCES Bertness, M.D. & Pennings, S.C. 2000. Spatial variation in process and pattern in salt marsh plant communities in eastern North America. In Weinstein, M.P. & Kreeger, D.A. (eds) Concepts and Controversies in Tidal Marsh Ecology : 39 – 57. Dordrecht: Kluwer Academic Publishers. Brown, A.F. & Atkinson, P.W. 1996. Habitat associations of coastal wintering passerines. Bird Study 43: 188 – 190. Burd, F. 1992. Erosion and Vegetation Change on the Saltmarshes of Essex and North Kent Between 1973 and 1988. Research and Survey in Nature Conservation 42. Peterborough: Nature Conservancy Council. Cahoon, D.R., French, J.R., Spencer, T., Reed, D.J. & Moller, I. 2000. Vertical accretion versus elevational adjustment in UK saltmarshes: an evaluation of alternative methodologies. In Pye, K. & Allen, J.R.L. (eds) Coastal and Estuarine Environments. Geol. Soc. Lond. Spec. Publ. 175: 223 – 238. Charman, K. & Macey, A. 1978. The winter grazing of saltmarsh vegetation by Dark-bellied Brent Geese. Wildfowl 29: 153 – 162. Daborn, G.R., Amos, C.L., Berlinsky, M., Christian, H., Drapeau, G., Faas, R.W., Grant, J., Long, B., Paterson, D.M., Perillo, G.M.E. & Piccolo, M.C. 1993. An ecological ‘cascade’ effect. Migratory birds affect stability of intertidal sediments. Limnol. Oceanogr. 38: 225 – 231. Davis, P. & Moss, D. 1984. Spartina and waders – the Dyfi estuary. In Doody, P. (ed.) Spartina anglica in Great Britain: 37–40. Peterborough: Nature Conservancy Council. Davy, A.J. 2000. Development and structure of salt marshes; community patterns in time and space. In Weinstein, M.P. & Kreeger, D.A. (eds) Concepts and Controversies in Tidal Marsh Ecology : 137–155. Dordrecht: Kluwer Academic Publishers. Dixon, A.M., Leggett, D.J. & Weight, R.C. 1998. Habitat creation opportunities for landward coastal realignment: Essex case studies. J. Chart. Inst. Water. Environ. Manage. 12: 107–112. Ferns, P.N. 1992. Bird Life of Coasts and Estuaries. Cambridge: Cambridge University Press. Frid, C.L.J., Chandrasekara, W.U. & Davey, P. 1999. The restoration of mud flats invaded by common cord-grass

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(Spartina anglica, C.E. Hubbard) using mechanical disturbance and its effects on the macrobenthic fauna. Aquat. Conserv. Mar. Freshw. Ecosyst. 9: 47 – 61. Funnell, B.M. & Pearson, I. 1989. Holocene sedimentation on the North Norfolk barrier coast in relation to sea-level change. J. Quat. Sci. 4: 25 – 36. Garbutt, R.A., Barratt, D.R., Myhill, D.G., Cox, R. & Rothery, P. 2000. Botanical and Accretional Studies at Tollesbury, Essex and Saltram Devon. Managed Realignment at Tollesbury and Saltram. Annual Report for 1999. Report C 00356. Monk’s Wood: Centre for Ecology and Hydrology. Goss-Custard, J.D. & Moser, M.E. 1988. Rates of change in the numbers of dunlin (Calidris alpina), wintering in British estuaries in relation to the spread of Spartina anglica. J. Appl. Ecol. 25: 95 – 109. Hughes, R.G. 1998. Saltmarsh erosion and management of saltmarsh restoration; the effects of infaunal invertebrates. Aquat. Conserv. Mar. Freshw. Ecosyst. 9: 83 – 95. Hughes, R.G. 2001. Biological and physical processes that affect saltmarsh erosion and saltmarsh restoration; development of hypotheses. Ecol. Stud. 151: 173 – 192. Hughes, R.G., Lloyd, D., Ball, L. & Emson, D. 2000. The effects of the polychaete Nereis diversicolor on the distribution and transplanting success of Zostera noltii. Helgol. Mar. Res. 54: 129 – 136. Hughes, R.G. & Paramor, O.A.L. 2004. On the loss of saltmarshes in South-east England and methods for their restoration. J. Appl. Ecol. 41: 440 – 448. Lane, S.J. & Hassall, M. 1996. Nocturnal feeding by Dark-bellied Brent Geese Branta Bernicla Bernicla. Ibis 138: 291–297. Long, S.P. & Mason, C.F. 1983. Saltmarsh Ecology. Glasgow: Blackie. Paramor, O.A.L. & Hughes, R.G. 2004. The effects of bioturbation and herbivory by the polychaete Nereis diversicolor on loss of saltmarsh in South-east England. J. Appl. Ecol. 41: 449 – 463. Post, D.M., Taylor, J.P., Kitchell, J.F., Olson, M.H., Schindler, D.E. & Herwig, B.R. 1998. The role of migratory waterfowl as nutrient vectors in a managed wetland. Conserv. Biol. 12: 910 – 920. Pye, K. 2000. Saltmarsh erosion in south east England. Mechanisms, causes and implications. In Sherwood, B.R., Gardiner, B.G. & Harris, T. (eds) British Saltmarshes: 359 – 396. London: Linnean Society of London. Raffaelli, D. 1999. Nutrient enrichment and trophic organisation in an estuarine food web. Acta Oecol. 20: 449 – 461. Rowcliffe, J.M., Watkinson, A.R., Sutherland, W.J. & Vickery, J.A. 1995. Cyclic winter grazing patterns in Brent Geese and the regrowth of salt-marsh grass. Funct. Ecol. 9: 931 – 941. Sullivan, M.J. & Currin, C.A. 2000. Community structure and functional dynamics of benthic microalgae in salt marshes. In Weinstein, M.P. & Kreeger, D.A. (eds) Concepts and Controversies in Tidal Marsh Ecology : 81 –106. Dordrecht: Kluwer Academic Publishers. Teal, J.M. & Howes, B.L. 2000. Salt marsh values; retrospection from the end of the century. In Weinstein, M.P. & Kreeger, D.A. (eds) Concepts and Controversies in Tidal Marsh Ecology : 9 – 19. Dordrecht: Kluwer Academic Publishers. Thomas, C. & Christian, R.R. 2001. Comparison of nitrogen cycling in saltmarsh zones related to sea level rise. Mar. Ecol. Prog. Ser. 221: 1 –16.


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Touchette, B.W. & Burkholder, J.M. 2000. Review of nitrogen and phosphorus metabolism in seagrasses. J. Exp. Mar. Biol. Ecol. 250: 133– 167. Underwood, G.J.C. & Kromkamp, J. 1999. Primary production by phytopklankton and microphytobenthos in estuaries. Adv. Ecol. Res. 29: 93 – 153. Valiela, I. 1984. Marine Ecological Processes. New York: Springer-Verlag.


Valiela, I., Cole, M.I., McClelland, J., Hauxwell, J., Cebrian, J. & Joye, S.B. 2000. Role of salt marshes as part of coastal landscapes. In Weinstein, M.P. & Kreeger, D.A. (eds) Concepts and Controversies in Tidal Marsh Ecology: 23 –38. Dordrecht: Kluwer Academic Publishers. Received 2 May 2002; revision accepted 8 March 2004.