Shellfish Dredging Pushes a Flexible Avian Top Predator out of a Marine Protected Area

There is a widespread concern about the direct and indirect effects of industrial fisheries; this concern is particularly pertinent for so-called “marine protected areas” (MPAs), which should be safeguarded by national and international law. The intertidal flats of the Dutch Wadden Sea are a State Nature Monument and are protected under the Ramsar convention and the European Union's Habitat and Birds Directives. Until 2004, the Dutch government granted permission for ~75% of the intertidal flats to be exploited by mechanical dredgers for edible cockles (Cerastoderma edule). Here we show that dredged areas belonged to the limited area of intertidal flats that were of sufficient quality for red knots (Calidris canutus islandica), a long-distance migrant molluscivore specialist, to feed. Dredging led to relatively lower settlement rates of cockles and also reduced their quality (ratio of flesh to shell). From 1998 to 2002, red knots increased gizzard mass to compensate for a gradual loss in shellfish quality, but this compensation was not sufficient and led to decreases in local survival. Therefore, the gradual destruction of the necessary intertidal resources explains both the loss of red knots from the Dutch Wadden Sea and the decline of the European wintering population. This study shows that MPAs that do not provide adequate protection from fishing may fail in their conservation objectives.

[1]  J. G. Hiddink,et al.  Effects of suction-dredging for cockles on non-target fauna in the Wadden Sea [rapid communication] , 2003 .

[2]  Theunis Piersma,et al.  Long‐term indirect effects of mechanical cockle‐dredging on intertidal bivalve stocks in the Wadden Sea , 2001 .

[3]  P. Atkinson,et al.  Changes in commercially fished shellfish stocks and shorebird populations in the Wash, England , 2003 .

[4]  K. Bjorndal,et al.  Historical Overfishing and the Recent Collapse of Coastal Ecosystems , 2001, Science.

[5]  T. Piersma,et al.  Time course and reversibility of changes in the gizzards of red knots alternately eating hard and soft food. , 2001, The Journal of experimental biology.

[6]  S. Nebel,et al.  Length of stopover, fuel storage and a sex-bias in the occurrence of red knots Calidris c. canutus and C-c. islandica in the Wadden Sea during southward migration , 2000 .

[7]  J. Goss-Custard,et al.  The Ecology of the Wash. I. Distribution and Diet of Wading Birds (Charadrii) , 1977 .

[8]  L. Zwarts,et al.  Why knot Calidris canutus take medium-sized Macoma balthica when six prey species are available , 1992 .

[9]  A. Prater The Ecology of Morecambe Bay. III. The Food and Feeding Habits of Knot (Calidris canutus L.) in Morecambe Bay , 1972 .

[10]  S. Nebel,et al.  Reversible size-changes in stomachs of shorebirds: when, to what extent, and why? , 1999 .

[11]  Theunis Piersma,et al.  Digestive bottleneck affects foraging decisions in red knots Calidris canutus. I. Prey choice , 2005 .

[12]  T. Surette,et al.  In Retrospect the Assumption of Sustainability for Atlantic Fisheries has Proved an Illusion , 2005, Reviews in Fish Biology and Fisheries.

[13]  C. J. Smit,et al.  Trends van benthivore watervogels in de Nederlandse Waddenzee 1975-2002: grote verschillen tussen schelpdiereneters en wormeneters , 2005 .

[14]  Leo R. M. Maas,et al.  A new pressure sensory mechanism for prey detection in birds: the use of principles of seabed dynamics? , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  G. Visser,et al.  Cost-benefit analysis of mollusc eating in a shorebird I. Foraging and processing costs estimated by the doubly labelled water method , 2003, Journal of Experimental Biology.

[16]  Theunis Piersma,et al.  Digestive bottleneck affects foraging decisions in red knots Calidris canutus. II. Patch choice and length of working day , 2005 .

[17]  G. Gudmundsson,et al.  Rapid Changes in the Size of Different Functional Organ and Muscle Groups during Refueling in a Long‐Distance Migrating Shorebird , 1999, Physiological and Biochemical Zoology.

[18]  A. Grant,et al.  Managed realignment in the UK – the first 5 years of colonization by birds , 2004 .

[19]  Hugh P. Possingham,et al.  Population models for marine reserve design: A retrospective and prospective synthesis , 2003 .

[20]  Pauline Kamermans,et al.  Mussel culture and cockle fisheries in The Netherlands: finfing a balance between economy and ecology , 2002 .

[21]  P. Battley,et al.  Modelling phenotypic flexibility : an optimality analysis of gizzard size in Red Knots Calidris canutus , 2006 .

[22]  S. Jameson,et al.  The three screen doors: can marine "protected" areas be effective? , 2002, Marine pollution bulletin.

[23]  N. J. Frost,et al.  Predicting site quality for shorebird communities:a case study on the Humber estuary, UK , 2005 .

[24]  H. Hirakawa Diet optimization with a nutrient or toxin constraint. , 1995, Theoretical population biology.

[25]  Simon Verhulst,et al.  Shellfish Fishery Severely Reduces Condition and Survival of Oystercatchers Despite Creation of Large Marine Protected Areas , 2004 .

[26]  P. Luttikhuizen,et al.  Morphological dynamics in the foraging apparatus of a deposit feeding marine bivalve: phenotypic plasticity and heritable effects , 2004 .

[27]  J. V. van Gils,et al.  Cost-benefit analysis of mollusc-eating in a shorebird II. Optimizing gizzard size in the face of seasonal demands , 2003, Journal of Experimental Biology.

[28]  B. Sandercock Estimation of survival rates for wader populations: a review of mark-recapture methods , 2003 .

[29]  P. Herman,et al.  Interspecific and intraspecific variation of δC and δN in deposit‐ and suspension‐feeding bivalves (Macoma balthica and Cerastoderma edule): Evidence of ontogenetic changes in feeding mode of Macoma balthica , 2004 .

[30]  L. Zwarts,et al.  How the food supply harvestable by waders in the Wadden Sea depends on the variation in energy density, body weight, biomass, burying depth and behaviour of tidal-flat invertebrates , 1993 .

[31]  P. Richard,et al.  Food sources of an infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oléron Bay, as determined by analyses of carbon and nitrogen stable isotopes , 1999 .

[32]  W. Sutherland,et al.  Depletion models can predict shorebird distribution at different spatial scales , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  Theunis Piersma,et al.  Reconstructing diet composition on the basis of faeces in a mollusc-eating wader, the Knot Calidris canutus , 1993 .

[34]  S. Verhulst,et al.  Estimating Organ Size in Small Migrating Shorebirds with Ultrasonography: An Intercalibration Exercise , 1999, Physiological and Biochemical Zoology.

[35]  D. Moss,et al.  Changes in fisheries practices and oystercatcher survival, recruitment and body mass in a marginal cockle fishery , 2005 .

[36]  J. Gils,et al.  Holling's functional response model as a tool to link the food-finding mechanism of a probing shorebird with its spatial distribution , 1995 .

[37]  Clive W. Anderson,et al.  Predicting the Distribution of Individuals and the Consequences of Habitat Loss: The Role of Prey Depletion , 1993 .

[38]  J. V. van Gils,et al.  Reinterpretation of gizzard sizes of red knots world-wide emphasises overriding importance of prey quality at migratory stopover sites , 2005, Proceedings of the Royal Society B: Biological Sciences.