Benefits to shorebirds from invasion of a non-native shellfish

Introductions of non-native species are seen as major threats to ecosystem function and biodiversity. However, invasions of aquatic habitats by non-native species are known to benefit generalist consumers that exhibit dietary switches and prey upon the exotic species in addition to or in preference to native ones. There is, however, little knowledge concerning the population-level implications of such dietary changes. Here, we show that the introduction of the Manila clam Tapes philippinarum into European coastal waters has presented the Eurasian oystercatcher Haematopus ostralegus ostralegus with a new food resource and resulted in a previously unknown predator–prey interaction between these species. We demonstrate, with an individuals-based simulation model, that the presence of this non-native shellfish, even at the current low density, has reduced the predicted over-winter mortality of oystercatchers at one recently invaded site. Further increases in clam population density are predicted to have even more pronounced effects on the density dependence of oystercatcher over-winter mortality. These results suggest that if the Manila clam were to spread around European coastal waters, a process which is likely to be facilitated by global warming, this could have considerable benefits for many shellfish-eating shorebird populations.

[1]  W. Thuiller,et al.  Predicting species distribution: offering more than simple habitat models. , 2005, Ecology letters.

[2]  P. Viaroli,et al.  Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro , 2001, Hydrobiologia.

[3]  J. P. Verdaat,et al.  Identification and size estimation of Spisula subtruncata and Ensis americanus from shell fragments in stomachs and faeces of Common Eiders Somateria mollissima and Common Eiders Scoters Melanitta nigra , 2007 .

[4]  Antonio Figueras Huerta,et al.  Brown ring disease and parasites in clams (Ruditapes decussatus and R. philippinarum) from Spain and Portugal , 1996 .

[5]  J. Humphreys,et al.  Population dynamics of naturalised Manila clams Ruditapes philippinarum in British coastal waters , 2007 .

[6]  M. Gatto,et al.  Density and temperature-dependence of vital rates in the Manila clam Tapes philippinarum: a stochastic demographic model , 2004 .

[7]  P. Worsfold,et al.  Characterisation of the South West European Marine Sites: Plymouth Sound and Estuaries cSAC, SPA. Occasional Publication of the Marine Biological Association 9 , 2003 .

[8]  P. Goulletquer,et al.  Marine Molluscan Production Trends in France: From Fisheries to Aquaculture , 1997 .

[9]  J. Beukema Expected changes in the wadden sea benthos in a warmer world: Lessons from periods with mild winters , 1992 .

[10]  A. Jensen,et al.  13. The Manila Clam in Poole Harbour , 2005 .

[11]  Susan L. Williams,et al.  Erratum: The impacts of climate change in coastal marine systems (Ecology Letters (2006) 9 (228-241)) , 2006 .

[12]  D. Whitfield Predation by Eurasian sparrowhawks produces density‐dependent mortality of wintering redshanks , 2003 .

[13]  John Humphreys,et al.  Naturalization of the Manila clam (Tapes philippinarum), an alien species, and establishment of a clam fishery within Poole Harbour, Dorset , 2004, Journal of the Marine Biological Association of the United Kingdom.

[14]  K. Rothhaupt,et al.  Strong impact of wintering waterbirds on zebra mussel (Dreissena polymorpha) populations at Lake Constance, Germany , 2005 .

[15]  N. Mieszkowska,et al.  Changes in the Range of Some Common Rocky Shore Species in Britain – A Response to Climate Change? , 2006, Hydrobiologia.

[16]  A. Lawrence,et al.  The effects of climate change on the reproduction of coastal invertebrates , 2004 .

[17]  J. Goss‐Custard The effect of migration and scale on the study of bird populations: 1991 Witherby Lecture , 1993 .

[18]  Richard A. Stillman,et al.  Modelling the effect of environmental change on shorebirds: A case study on Poole Harbour, UK , 2006 .

[19]  L. Zwarts,et al.  Seasonal and annual variation in body weight, nutrient stores and mortality of Oystercatchers Haematopus ostralegus , 1996 .

[20]  R. Stillman,et al.  7. Macro-invertebrate fauna in the intertidal mudflats , 2005 .

[21]  C. Solidoro,et al.  Ecological and economic considerations on fishing and rearing of Tapes phillipinarum in the lagoon of Venice , 2003 .

[22]  Robin A. Clark,et al.  Non-native Marine Species in British Waters: A Review and Directory , 1997 .

[23]  Y. Paulet,et al.  Reproductive pattern of the clams, Ruditapes decussatus and R. philippinarum on intertidal flats in Brittany , 1994, Journal of the Marine Biological Association of the United Kingdom.

[24]  A. Bodoy,et al.  Croissance comparée de la palourde européenne (Ruditapes decussatus) et de la palourde japonaise (Ruditapes philippinarum) dans un écosystème artificiel méditerranéen , 1980 .

[25]  R. B. Jackson,et al.  Global biodiversity scenarios for the year 2100. , 2000, Science.

[26]  I. Laing,et al.  The physiology and biochemistry of diploid and triploid Manila clam (Tapes philippinarum Adams & Reeve) larvae and juveniles , 1994 .

[27]  D. Razet,et al.  Ecophysiologie et bilan énergétique de la palourde japonaise d'élevage Ruditapes philippinarum , 1989 .

[28]  J. E. Byers MARINE RESERVES ENHANCE ABUNDANCE BUT NOT COMPETITIVE IMPACTS OF A HARVESTED NONINDIGENOUS SPECIES , 2005 .

[29]  J. Lovvorn,et al.  RELATIVE FORAGING VALUE TO LESSER SCAUP DUCKS OF NATIVE AND EXOTIC CLAMS FROM SAN FRANCISCO BAY , 2004 .

[30]  R. Bailey,et al.  PREDATION OF ZEBRA MUSSELS BY DIVING DUCKS: AN EXCLOSURE STUDY' , 1994 .

[31]  Richard A. Stillman,et al.  The Burry shellfishery and oystercatchers: using a behaviour-based model to advise on shellfishery management policy , 2003 .

[32]  Richard A. Stillman,et al.  INDIVIDUAL‐BASED MODELS AND THE MANAGEMENT OF SHOREBIRD POPULATIONS , 2008 .

[33]  S. Galatowitsch Invasive aquatic species of Europe , 2004 .

[34]  Stephan Gollasch,et al.  Invasive Aquatic Species of Europe. Distribution, Impacts and Management , 2002, Springer Netherlands.

[35]  P. Breber Introduction and Acclimatisation of the Pacific Carpet Clam, Tapes Philippinarum, To Italian Waters , 2002 .

[36]  W. Suter Der Einfluss von Wasservögeln auf Populationen der Wandermuschel (Dreissena polymorpha Pall.) am Untersee/Hochrhein (Bodensee) , 1982, Schweizerische Zeitschrift für Hydrologie.

[37]  T. Piersma,et al.  Numbers, midwinter distribution, and migration of wader populations using the East Atlantic flyway , 1994 .

[38]  Philippe Goulletquer,et al.  A bibliography of the Manila clam Tapes philippinarum , 1997 .

[39]  H. Mooney,et al.  The evolutionary impact of invasive species , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R. H. Smith,et al.  BEHAVIOURAL ECOLOGY ECOLOGICAL CONSEQUENCES OF ADAPTIVE BEHAVIOUR , 2007 .

[41]  References , 1971 .

[42]  B. Ens,et al.  Causes of variation in prey profitability and its consequences for the intake rate of the Oystercatcher Haematopus ostralegus , 1996 .

[43]  G. Austin,et al.  Shifting nonbreeding distributions of migratory fauna in relation to climatic change , 2005 .

[44]  A. O. Ambrogi Biotic Invasions in a Mediterranean Lagoon , 2000, Biological Invasions.

[45]  J. Goss‐Custard,et al.  Field tests of the accuracy of estimating prey size from bill length in oystercatchers, Haematopus ostralegus, eating mussels, Mytilus edulis , 1987, Animal Behaviour.

[46]  S. Hawkins,et al.  Predicting the effects of marine climate change on the invertebrate prey of the birds of rocky shores , 2004 .

[47]  A. Occhipinti‐Ambrogi,et al.  Biological invasions as a component of global change in stressed marine ecosystems. , 2003, Marine pollution bulletin.

[48]  R. Uncles,et al.  Site Characterisation of the South West European Marine Sites: Fal and Helford cSAC , 2003 .