5.1 Shellfishing and oystercatchers The largest numbers of birds that depend on commercially exploited shellfish occur in Europe during autumn and winter, over which period the birds must survive in good condition in order to migrate to the breeding grounds in spring. Although the birds can eat other prey species when shellfish stocks are low, these alternatives often do not allow birds to survive as well, and in such good body condition, as when shellfish are abundant (Camphuysen et al. [1996, 2002], Smit et al. , Atkinson et al. ). As a result, the size of the oystercatcher population wintering in the Wash, UK, for example, decreased sharply over the 1990s when shellfish stocks were frequently very low (Atkinson et al. ). Even more precipitous declines in the numbers of mollusc-eating birds (oystercatcher, knot Calidris canutus, eider duck Somateria mollissima) occurred in the Dutch Wadden Sea where winter shellfish stocks have frequently been at very low levels over the last 2 decades (Beukema and Cadée ).
If bird populations are to be maintained, sufficient shellfish to meet their demands must remain for them after harvesting. But the question then is what constitutes sufficient shellfish? A common approach has been to base this decision on the biomass of shellfish required by the whole bird population to satisfy its energy demands (Lambeck et al. ). One oystercatcher requires approximately 10 kg AFDM of shellfish flesh to satisfy its energy requirements from autumn to spring (Stillman et al. ). Ten thousand birds would therefore consume 100,000 kg (AFDM) by spring, equivalent to approximately 3,000 tons of shellfish wet weight (including shells).
But as the model of Exe estuary oystercatchers showed, it may take considerably more than 10 kg AFDM per bird to ensure that oystercatchers survive the winter in good condition (Figure 6). This finding was confirmed when the shorebird IBM was applied to a further four European oystercatcher–shellfish systems (Figure 12). As on the Exe estuary, the probability of oystercatchers starving in these four systems was extremely low and independent of shellfish stock at the high shellfish abundance of 70–120 kg AFDM/bird (Goss-Custard et al. ). It increased sharply below this range with the increase beginning over the range 20–61 kg AFDM/bird, depending on the system. The increase seemed to begin earlier where mussels, rather than cockles Cerastoderma edule, were the predominant shellfish (Figure 12).
Figure 12. The critical threshold, or ecological requirement, for shellfish that is needed by a single oystercatcher arriving in autumn on a sample of European estuaries if it is to survive until the following spring.
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The data show that, to ensure that most oystercatchers survive until spring, there must be present at the time of their arrival in autumn from two to six times the amount of shellfish that oystercatchers actually eat, even though they can and frequently do take alternative prey. In other words, the “ecological food requirement” greatly exceeds the “physiological requirement.” Reductions in shellfish biomass available per oystercatcher increases mortality rate (and reduces the birds' body condition) by simultaneously increasing the intensity of interference competition and the rate of food depletion.
To maintain oystercatcher populations in areas harvested for shellfish, stocks must not be allowed to fall below two to six times the shellfish biomass that the birds consume. Providing enough food to meet their physiological requirement is simply not enough. Until recently, the policy in The Netherlands for regulating shellfishing on their important tidal flats was to ensure that 60% of the food requirements of mollusc-eating birds, such as the oystercatcher, remained after harvesting, on the grounds that the remaining consumption would be provided by alternative prey, such as polychaete worms and other bivalves. We now know that this provision was inadequate by a factor of three- to tenfold and accounted for the decline in the numbers of these birds in The Netherlands that has occurred over the last 2 decades. The policy has now changed so that a much more of the shellfish stocks are reserved for the birds.
Recent work with the shorebird IBM has shown how shellfishing policy can be formulated in such a way as not only to improve the feeding conditions of the birds but also simultaneously to increase the yield to the shellfishery (Caldow et al. ).
At the Menai Strait in north Wales, the overwinter consumption of 242 tons of commercially harvestable mussels (>40 mm) by oystercatchers in 1999–2000 was worth £133,000 ($226,000), which represented 19% of the value of the landings. Traditionally, the shellfishery operates by dredging young mussels in their first year of life (the “seed mussels”) from the sublittoral and laying them onto commercial lays in the intertidal zone where they can be tended and subsequently harvested but where they are very vulnerable to frequent attack by oystercatchers. An IBM of this system showed that the losses to oystercatchers of the largest and commercially harvestable mussels could be considerably reduced by repeatedly changing the shore level at which the mussels were situated at different stages of their development from seed mussels to harvestable adults (Caldow et al. ).
Caldow et al.  proposed that the seed mussels should first be laid upshore where losses to oystercatchers would only be slight because most oystercatchers do most of their feeding at the middle and low shore levels where larger mussels with a high flesh-content occur. Even though the mussels are small, very few could be eaten at these higher shore levels by sublittoral predators, such as crabs Carcinus maenas, which can inflict enormous damage on young mussels in the sublittoral zone. As the seed-mussels grow over the next 2 to 3 years, they should be moved progressively further downshore where the growing conditions are better: downshore, the mussels are covered by water, and so able to feed for a greater proportion of the time. This would be the stage at which the mussels would be most at risk from oystercatchers because of their relatively high flesh content, and thus high food value to the birds, and frequent exposure to the birds over the low tide period. The mussels would spend their last season before being harvested very far down the shore where, by virtue of being covered by the tide for so much of the time, their growth rates and flesh content would be further increased. By that stage in their development, the mussels would be large enough to avoid most of the predation from crabs that, at earlier stages, would have taken so many of them. Although these large mussels would be very attractive to oystercatchers, the birds would consume very few of them because, at these very low shore levels, the mussels would only seldom be exposed over dead low water to predation by birds.
The results suggested that adopting this management practice would increase the return to the commercial fishery from the seed mussels by up to fourfold even though it would mean that more mussels would be lost to oystercatchers during the early stages of the cultivation process. By accepting greater losses of mussels earlier in the cultivation cycle, rather than later as at present, not only would the yield to the fishery be increased but also the feeding conditions for oystercatchers would be improved. Caldow et al.  concluded with the encouraging message that, with appropriate management, the interest of shellfish growers and competing shorebirds do not necessarily have to conflict but can both benefit simultaneously from a change in shellfishery management practice.
5.2 Disturbance from people and raptors Disturbance causes birds to spend energy flying away and to lose feeding time while relocating to different feeding areas, where the increased bird densities may intensify competition from interference and, if of sufficient duration, from increased rates of prey depletion. The shorebird IBM has been used to investigate whether disturbance from people walking on the mussel beds of the Exe estuary could or already does reduce the fitness of oystercatchers and to explore ways of regulating disturbance so that it has no effect on the birds (West et al. ). Here we show how the shorebird IBM can also be used to establish how frequently shorebirds can be put to flight before their fitness is affected and to establish simple policies for managing disturbance.
Goss-Custard et al.  showed how IBMs can be used to establish “critical thresholds” for the frequency with which shorebirds can be disturbed before their chances of dying of starvation are significantly increased. By way of an example, they used oystercatchers wintering in the Reserve Naturelle of the baie de Somme, France where oystercatchers start the winter eating cockles but switch to other prey, such as the polychaete worm Nereis diversicolor, if the cockles disappear later in the winter, mainly through storms.
Field studies in the baie de Somme showed that oystercatchers were disturbed into flight up to 0.513–1.73 times per daylight hour by people and over-flying raptors, depending on the winter. As Figure 13 indicates, simulations with the IBM showed that the highest disturbance frequency would only have increased mortality by a small amount in the winter of 1995–1996, a mild winter in which cockles remained abundant throughout. Most birds could continue eating cockles throughout that winter and did not have to switch to the less profitable ragworms. In contrast, in the similarly mild winter of 1997–1998 during which most cockles disappeared, mortality started to increase at 0.5–0.6 disturbances/daylight hour, frequencies of disturbance that were common on the baie de Somme (Figure 13). The critical disturbance threshold was only 0.2–0.3 disturbances/daylight-hour in 1996–1997, the third winter modeled, when, in addition to cockles becoming depleted, a prolonged period of cold weather occurred in January and many birds arrived from The Netherlands where many of the intertidal flats were ice covered (Hulscher et al. ).
Figure 13. The effect of the frequency with which oystercatchers are put to flight on the baie de Somme on their overwinter mortality rate in a mild and a severe winter. The vertical arrows show the frequencies with which oystercatchers were observed to be put to flight by people over three winters: in 1997/1998, the frequency with which they were disturbed by raptors flying over head was also recorded.
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The critical disturbance thresholds were similar whether the disturbances were caused by people staying for 20 minutes or by rapidly over-flying raptors (Goss-Custard et al. ). Therefore, a quite simple policy rule can be devised for the management of disturbance in the Reserve. A frequency of flying caused by people and/or raptors in autumn and early winter of <1.5/daylight hour can be allowed. However, if the cockles become considerably depleted by the end of December, especially if they are small, the frequency of disturbance—from both people and raptors—should be kept below 0.5/hour. This could mean that in winters with many raptors, people should not be allowed to disturb the birds at all. Similarly, no disturbance from people should be allowed during prolonged cold spells.
This policy guideline is practicable for the baie de Somme. It is very easy to detect from a very simple sampling program when cockles become scarce. It is also straightforward to estimate the frequency with which birds are put to flight by people or by raptors. Although it is of course impossible to control the number of disturbances due to raptors, it is possible to see when the disturbance from people causes the total number of disturbances from raptors and people to exceed the critical threshold, whereupon access to the feeding areas by people can then be stopped. Similarly, it is easy to prevent access by people during cold spells, just as hunting and catching birds is also prevented during periods of severe winter weather.
This example of the baie de Somme has shown that IBMs can be used to establish practicable critical disturbance thresholds, as well as to predict the effect of existing frequencies of disturbance on a particular estuary as shown by West et al. . The level of the critical threshold will depend, of course, on estuary-specific features, and the same values cannot be regarded as being applicable everywhere. The precise value of the critical thresholds will depend on the bird species and the many factors known to affect the ability of shorebirds to survive the winter in good condition. But by using the oystercatchers of the baie de Somme as the test system, Goss-Custard et al.  have demonstrated that IBMs provide a means by which critical disturbance thresholds can, for the first time, be obtained.
5.3 Spread of the grass Spartina onto upshore mudflats In many parts of the world, the spread of cord grass Spartina spp. onto mudflats is believed to threaten the shorebirds that feed on the high-level mudflats that expose first on the ebbing tide and are covered last as the tide flows back. By covering the mudflat with vegetation among which many birds will not or cannot forage, spreading Spartina not only removes an area of food supply but may also reduce the amount of foraging time available to shorebirds by preventing them from feeding at the start and end of the exposure period. There is some evidence to suggest that the numbers of wintering dunlin Calidris alpina decreased in those British estuaries where Spartina had spread extensively but remained stable in those where the grass had not spread (Goss-Custard and Moser ). The causality of this correlation has, of course, been questioned because it is uncertain whether it was the spread of the Spartina itself or the changes in the estuary environment that encouraged the spread of the grass that was responsible for the decrease in dunlin numbers (Goss-Custard and Moser ). Further tests are needed to investigate the impact of Spartina, if any, on shorebirds that feed on high level mudflats.
A recent IBM of dunlin feeding in the baie de Somme, France, has provided modeling evidence that Spartina can indeed reduce shorebird fitness (S.E.A. le V. dit Durell, unpublished information). Dunlin feed on the upper mudflats over which Spartina has been spreading in recent years at an annual rate of 20–40 m. The shorebird IBM showed that, at such a rate of spread, the fitness of dunlin begins to be reduced after only a few years and that their mortality rate could double after only 10 years of Spartina spread (Figure 14). This happens even though the food supply and duration of the exposure period elsewhere remains the same, suggesting that Spartina should be removed if a reduction in dunlin fitness is to be avoided.
Figure 14. The overwinter mortality rate of dunlin on the baie de Somme as a function of the number of years in which Spartina has been spreading downshore onto the feeding grounds of the birds. The feeding area removed by the spread of the grass is also shown.
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5.4 Habitat loss, sea-level rise, and mitigation The intertidal feeding areas of shorebirds are reduced when they are covered by various developments, raising concern that this reduces the fitness of shorebirds by reducing the extent of their food supplies. When this happens in some parts of the world, the law requires that effective mitigation be provided to remove the potential threat from the development to the birds. Until recently, however, there was no means by which the effectiveness of any proposed mitigating measure could be tested. Indeed, there was no means to establish whether the birds would be affected by the habitat loss in the first place and so whether the mitigation—which may be very expensive—was even required.
An IBM of dunlin wintering on the Seine estuary illustrates how the shorebird IBM can both explore whether habitat loss will reduce shorebird fitness and, if so, whether a proposed mitigation would be effective at returning fitness to its previous level (Durell et al. [2004; 2005]). The proposal was to extend the port at Le Havre at the mouth of the Seine onto 105 ha of intertidal mudflats and to provide by way of mitigation an area of mudflat further upstream by removing vegetation from an area of mudflat, which would allow the birds to feed there (Figure 15). This would provide an area of upshore mudflat of comparable quality to that which was lost under the port development. The IBM of this system showed that the initial loss of the mudflat under the port development would indeed be likely to increase the winter mortality rate of the dunlin. It also shows that an equivalent area of mudflat would have to be freed from vegetation for it to be returned to its previous level (Figure 16). This can easily be understood. Because the loss of habitat was predicted to increase the mortality rate of the birds, mortality must be density dependent. Therefore, to return the mortality rate to its preport level, an equivalent area of habitat of a comparable quality to that which is lost must be provided. The policy advice emerging from this study, therefore, was that it was necessary to clear about 100 ha of vegetation if the proposed mitigation was to be fully effective.
Figure 15. Schematic diagram of the extension of the port at le Havre onto the feeding grounds of shorebirds wintering in the baie de Seine. The site of the proposed replacement mudflat is also shown.
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Figure 16. How an extension of the port at le Havre would affect the fitness of dunlin wintering on the baie de Seine, as predicted by the IBM. (A) Overwinter mortality rate. (B) The percentage of survivors failing to reach at least 75% of their target body mass by the end of the winter. The bars show the predicted rates before and after the port is extended and if replacement mudflats (either 50 or 100 ha) were to be provided by way of mitigation.
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Stillman et al.  used a multispecies version of the shorebird IBM to predict how a loss of intertidal habitat resulting from sea-level rise in the Humber estuary, UK, would affect the overwinter survival of nine shorebird species; dunlin, common ringed plover Charadrius hiaticula, red knot Calidris canutus, common redshank Tringa totanus, gray plover Pluvialis squatarola, black-tailed godwit Limosa limosa, bar-tailed godwit L. lapponica, Eurasian oystercatcher, and Eurasian curlew Numenius arquata. This model extended the previous shorebird IBM by predicting survival rates in a community of interacting species, and not just in a single species. Stillman et al.  found that shorebird survival was most strongly influenced by the biomass densities of annelid worms and of the bivalve molluscs the cockle and clam Macoma balthica. A 2–8% reduction in intertidal area (the magnitude expected through sea-level rise and industrial developments) decreased predicted survival rates of all species except dunlin, common ringed plover, red knot, and Eurasian oystercatcher.
5.5 Measuring and monitoring habitat quality for shorebirds Conservation managers responsible for estuaries are often required to monitor their site to ensure that the conservation status of any bird species for which the site is considered important is not affected by deterioration of their habitat or by disturbance of the birds themselves. For example, in Europe, the EU Habitats Directive 92/43/EEC, Article 6 states: “Member States shall take appropriate steps to avoid, in the special areas of conservation, the deterioration of natural habitats and the habitats of species as well as disturbance of the species for which the areas have been designated, in so far as such disturbance could be significant eg … .”
The conservation importance of an estuary is usually measured in terms of the numbers of birds using it, but monitoring bird numbers on an estuary is not in itself a reliable way of assessing whether the quality of a site is beginning to fall. There may be a lag between a decline in habitat quality and a detectable fall in bird numbers, particularly in long-lived species because established birds may be reluctant to change site. More importantly, the numbers of a bird species on a particular site depend not only on the conditions in that site but also on conditions elsewhere in the species' nonbreeding range and on the breeding grounds (Goss-Custard ). A decline in bird numbers at one site might be due to a decline in the quality of that site but it might also be caused by an increase in the quality of sites elsewhere in the nonbreeding range. A decline in the reproductive rate or an increase in mortality on the breeding grounds would reduce the size of the greater population to which the birds belong and hence could, in turn, reduce the number of birds using the site, even though its quality had not changed.
As bird numbers are not a reliable way to assess the quality of a site, another method is required. In migratory shorebirds population size is a function of the interaction between (i) the mortality and reproductive rates in the breeding ranges and (ii) the mortality rate in the nonbreeding range, including migratory routes (Goss-Custard [1980, 1981, 1993], Goss-Custard and Durell , Goss-Custard et al. [1995d, 1996b]). Because the objective of shorebird conservation in the nonbreeding range is to maintain the conservation status of birds, the best measure of habitat quality for an estuary is one that, directly or indirectly, determines these demographic rates. For migratory shorebirds during the nonbreeding season, this means that habitat quality should be measured in terms of its effect on the number of birds that die of starvation during the nonbreeding season, perhaps especially during severe winter weather. If it can be shown that feeding conditions in the site are sufficient to maintain present-day rates of survival at the current bird population size and in the current climatic conditions, then the quality of the estuary is being maintained. If the population using the estuary declines despite this, then the cause of that decline needs to be sought elsewhere.
West et al. demonstrated how a multispecies shorebird IBM could be used to assess the quality of the Wash estuary, UK, for eight overwintering shorebird species. The results identified the prey species that were most important for maintaining the present-day survival rates of the birds. Birds began to starve when the estuary-wide food biomass density in autumn fell below about 5 g AFDM m−2. Survival rates fell below 90% by the time prey biomass declined to 4 g AFDM m−2 (Figure 17). West et al. therefore suggested that the quality of the Wash estuary for shorebirds could be monitored by regular surveys of the food supply designed to establish whether the food supply had fallen below the 99% confidence limit of the biomass density required to maintain the present-day rates of survival (Figure 17). They also concluded that, as the survival of all species in the model remained high until there were as many as 20 disturbances per hour, the present low frequency of disturbance on the Wash does not threaten their survival. Importantly for estuary management, West et al. concluded that, for the Wash, prey density was a more important factor in shorebird survival than habitat area, and therefore habitat loss, and identified those shorebird species that were most vulnerable to changes in site quality.
Figure 17. Predicted effect of changes in prey biomass density on the percentage overwinter survival rate of shorebirds in the Wash embayment. The model was either run with all species simultaneously competing for prey (black symbols) or with single species, ignoring intraspecific competition (open symbols). For each bird species, prey biomass is the estuary-wide mean biomass density of their principal prey species within the size ranges consumed. The black vertical lines show the mean prey biomass estimated by a field survey, whereas the dark and light gray shading shows the 95% and 99% confidence limits of the survey, respectively.
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