Shorebirds as Integrators and Indicators of Mudflat Ecology

  • Kimberley J. MathotEmail author
  • Theunis Piersma
  • Robert W. Elner
Part of the Aquatic Ecology Series book series (AQEC, volume 7)


Shorebirds are major, but thus far under-acknowledged, players in mudflat food webs and associated physio-chemical processes. Mud is a critical habitat type for shorebirds, offering a multi-dimensional matrix of feeding opportunities through space and time. Shorebirds have evolved a spectrum of foraging modes with associated morphologies, and sensory and physiological adaptations which exploit these foraging opportunities. Although shorebirds are mud specialists and sentinels of mudflat ecosystem functioning, they have not yet been well integrated into the “mud club”. In this chapter, we highlight the key roles shorebirds play in food webs, and in physical and chemical processes within mudflat ecosystems. We illustrate how shorebird distribution and behaviour provides a mirror of mudflat ecology because their foraging behaviour reflects the underlying ecological conditions, including temporal and spatial patterns in food/community structure in and across mud. In particular, shorebirds may be important indicators of essential fatty acid production by diatoms in epibenthic biofilm fields covering muddy intertidal flats, especially in estuaries. We conclude by highlighting the major challenges facing shorebirds today and call for a paradigm shift in shorebird conservation, based on recreating and restoring intertidal mud ecosystems.


  1. Admiraal W, Peletier H (1980) Influence of seasonal variations of temperature and light on the growth rate of cultures and natural populations of intertidal diatoms. Mar Ecol Prog Ser 2:35–43CrossRefGoogle Scholar
  2. Ahmedou Salem MV, van der Geest M, Piersma T, Saoud Y, van Gils JA (2014) Seasonal changes in mollusc abundance in a tropical intertidal ecosystem, banc d’Arguin (Mauritania): testing the ‘depletion by shorebirds’ hypothesis. Estuar Coast Shelf Sci 136:26–34CrossRefGoogle Scholar
  3. Altenburg W, Engelmoer M, Mes R, Piersma T (1982) Wintering waders on the banc d’Arguin, Mauritania. Stichting Veth tot steun aan Waddenonderzoek, Leiden, 283 pGoogle Scholar
  4. Alves JA, Sutherland WJ, Gill JA (2012) Will improving wastewater treatment impact shorebirds? Effects of sewage discharges on estuarine invertebrates and birds. Anim Conserv 15:44–52CrossRefGoogle Scholar
  5. Amano T, Székely T, Koyama K, Amano H, Sutherland WJ (2010) A framework for monitoring the status of populations: an example from wader populations in the east Asian–Australasian flyway. Biol Conserv 143:2238–2247CrossRefGoogle Scholar
  6. Arts MT, Brett MT, Kains MJ (2009) Lipids in aquatic ecosystems. Springer, New York, 380 pGoogle Scholar
  7. Atkinson PW, Maclean IMD, Clark NA (2010) Impacts of shellfisheries and nutrient inputs on waterbird communities in the wash, England. J Appl Ecol 47:191–199CrossRefGoogle Scholar
  8. Baker AJ, González PM, Piersma T, Niles LJ, Serrano do Nascimento IdL, Atkinson PW, Clark NA, Minton CDT, Peck MK, Aarts G (2004) Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proc R Soc B 271:875–882Google Scholar
  9. Barbeau MA, Grecian LA, Arnold EE, Sheahan DC, Hamilton DJ (2009) Spatial and temporal variation in the population dynamics of the intertidal amphipod Corophium volutator in the upper bay of Fundy, Canada. J Crustac Biol 29:491–506CrossRefGoogle Scholar
  10. Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193CrossRefGoogle Scholar
  11. Barbosa A, Moreno E (1999) Evolution of foraging strategies in shorebirds: an ecomorphological approach. Auk 116:712–725CrossRefGoogle Scholar
  12. Battley PF, Piersma T (2005a) Adaptive interplay between feeding ecology and features of the digestive tract in birds. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 201–228Google Scholar
  13. Battley PF, Piersma T (2005b) Body composition and flight ranges of bar-tailed godwits (Limosa lapponica baueri) from New Zealand. Auk 122:922–937CrossRefGoogle Scholar
  14. Battley PF, Warnock N, Tibbitts TL, Gill RE, Piersma T, Hassell CJ, Douglas DC, Mulcahy DM, Gartrell BD, Schuckard R, Melville DS, Riegen AC (2012) Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J Avian Biol 43:21–32CrossRefGoogle Scholar
  15. Beck MW, Heck JKL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ, Sheridan PF, Weinstein MP (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51:633–641CrossRefGoogle Scholar
  16. Beninger PG, Elner RW, Morançais M, Decottignies P (2011) Downward trophic shift during breeding migration in the shorebird Calidris mauri (western sandpiper). Mar Ecol Prog Ser 428:259–269CrossRefGoogle Scholar
  17. Beukema JJ, Essink K, Michaelis H, Zwarts L (1993) Year-to-year variability in the biomass of macrobenthic animals on tidal flats of the Wadden Sea: how predictable is this food source for birds? Neth J Sea Res 31(4):319–330CrossRefGoogle Scholar
  18. Bijleveld AI, Twietmeyer S, Piechocki J, van Gils JA, Piersma T (2015) Natural selection by pulsed predation: survival of the thickest. Ecology 96:1943–1956PubMedCrossRefPubMedCentralGoogle Scholar
  19. Bijleveld AI, MacCurdy RB, Chan Y-C, Penning E, Gabrielson RM, Cluderay J, Spaulding EL, Dekinga A, Holthuijsen S, ten Horn J, Brugge M, van Gils JA, Winkler DW, Piersma T (2016) Understanding spatial distributions: negative density-dependence in prey causes predators to trade-off prey quantity with quality. Proc R Soc B 283:20151557PubMedCrossRefPubMedCentralGoogle Scholar
  20. Bocher P, Piersma T, Dekinga A, Kraan C, Yates MG, Guyot T, Folmer EO, Radenac G (2007) Site- and species-specific distribution patterns of molluscs at five intertidal soft-sediment areas in Northwest Europe during a single winter. Mar Biol 151:577–594CrossRefGoogle Scholar
  21. Boere GC, Piersma T (2012) Flyway protection and the predicament of our migrant birds. Ocean Coast Manag 68:157–168CrossRefGoogle Scholar
  22. Bom RA, de Fouw J, Klaassen RHG, Piersma T, Lavaleye MSS, Ens BJ, Oudman T, van Gils JA (2018) Food web consequences of an evolutionary arms race: molluscs subject to crab predation on intertidal mudflats in Oman are unavailable to shorebirds. J Biogeogr 45:342–354CrossRefGoogle Scholar
  23. Butler RW, Vermeer K (1994) The abundance of distribution of estuarine birds in the strait of Georgia, British Columbia. Can Wildl Serv Occas Paper 83:78 ppGoogle Scholar
  24. Butler RW, Delgado F, De La Cueva HC, Pulido V, Sandercock BK (1996) Migration routes of the western sandpiper. Wilson Bull 108:662–672Google Scholar
  25. Butler RW, Davidson NC, Morrison RIG (2001) Global-scale shorebird distribution in relation to productivity of near-shore oceans. Waterbirds 24:224–232CrossRefGoogle Scholar
  26. Campredon P (2000) Between the Sahara and the Atlantic. Banc d’Arguin National Park. Fondation Internationale du Banc d’Arguin, Arles, 121 pGoogle Scholar
  27. Carlier A, Chauvaud L, van der Geest M, Le Loc’h F, Le Duff M, Vernet M, Raffray J, Diakhaté D, Labrosse P, Wagué A, Le Goff C, Gohin F, Chapron B, Clavier J (2015) Trophic connectivity between offshore upwelling and the inshore food web of banc d’Arguin (Mauritania): new insights from isotopic analysis. Estuar Coast Shelf Sci 165:149–158CrossRefGoogle Scholar
  28. Catry T, Lourenço PM, Lopes RJ, Carneiro C, Alves JA, Costa J, Rguibi-Idrissi H, Bearhop S, Piersma T, Granadeiro JP (2016) Structure and functioning of intertidal food webs along an avian flyway: a comparative approach using stable isotopes. Funct Ecol 30:468–478CrossRefGoogle Scholar
  29. Christianen MJA, Middelburg JJ, Holthuijsen SJ, Jouta J, Compton TJ, van der Heide T, Piersma T, Sinninghe Damsté JS, van der Veer HW, Schouten S, Olff H (2017) Benthic primary producers are key to sustain the Wadden Sea food web: stable carbon isotope analysis at landscape scale. Ecology 98:1498–1512PubMedCrossRefPubMedCentralGoogle Scholar
  30. Clemens RS, Rogers DI, Hansen BD, Gosbell K, Minton CDT, Straw P, Bamford M, Woehler EJ, Milton DA, Weston MA, Venables B, Weller D, Hassell C, Rutherford B, Onton K, Herrod A, Studds CE, Choi CY, Dhanjal-Adams KL, Murray NJ, Skilleter GA, Fuller RA (2016) Continental-scale decreases in shorebird populations in Australia. Emu 116:119–135CrossRefGoogle Scholar
  31. Colombo SM, Wacker A, Parrish CC, Kainz MJ, Arts MT (2016) A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems. Environ Rev 25:163–174CrossRefGoogle Scholar
  32. Colwell MA (2010) Shorebird ecology, conservation, and management. University of California Press, Berkeley, 344 pGoogle Scholar
  33. Compton TJ, Bodnar W, Koolhaas A, Dekinga A, Holthuijsen S, ten Horn J, McSweeney N, van Gils JA, Piersma T (2016) Burrowing behavior of a deposit feeding bivalve predicts change in intertidal ecosystem state. Front Ecol Evol 4:19CrossRefGoogle Scholar
  34. Cooke BC, Jones AR, Goodwin ID, Bishop MJ (2012) Nourishment practices on Australian sandy beaches: a review. J Environ Manag 113:319–327CrossRefGoogle Scholar
  35. Cresswell W (1993) Escape responses by redshanks, Tringa totanus, on attack by avian predators. Anim Behav 46:609–611CrossRefGoogle Scholar
  36. Daborn GR, Amos CL, Brylinsky M, Christian H, Drapeau G, Faas RW, Grant J, Long B, Paterson DM, Perillo GME, Piccolo MC (1993) An ecological cascade effect: migratory birds affect the stability of intertidal sediments. Limnol Oceanogr 38:225–231CrossRefGoogle Scholar
  37. de Fouw J, van der Heide T, Oudman T, Maas LRM, Piersma T, van Gils JA (2016) Structurally complex sea grass obstructs the sixth sense of a specialized avian molluscivore. Anim Behav 115:55–67CrossRefGoogle Scholar
  38. Dekker D, Ydenberg R (2004) Raptor predation on wintering dunlins in relation to the tidal cycle. Condor 106:415–419CrossRefGoogle Scholar
  39. Deppe F (1999) Intertidal mudflats worldwide. Common Wadden Sea Secretariat (CWSS), Wilhelmshaven, 100 pGoogle Scholar
  40. Drever MC, Lemon MJF, Butler RW, Millikin RL (2014) Monitoring populations of western sandpipers and Pacific dunlins during northward migration on the Fraser River Delta, British Columbia, 1991–2013. J Field Ornithol 85:10–22CrossRefGoogle Scholar
  41. Du H, Sun L, Peng W, Hu J, Bao Z (2010) Sixteen polymorphic microsatellite markers for the mud snail, Bullacta exarata (Philippi, 1848). Conserv Genet Resour 2:23–25CrossRefGoogle Scholar
  42. Duerksen SW, Thiemann GW, Budge SM, Poulin M, Niemi A, Michel C (2014) Large, omega-3 rich, pelagic diatoms under Arctic Sea ice: sources and implications for food webs. PLoS One 9:18CrossRefGoogle Scholar
  43. Duijns S, van Gils JA, Spaans B, ten Horn J, Brugge M, Piersma T (2014) Sex-specific winter distribution in a sexually dimorphic shorebird is explained by resource partitioning. Ecol Evol 4:4009–4018PubMedPubMedCentralCrossRefGoogle Scholar
  44. Duijns S, van Gils JA, Smart J, Piersma T (2015) Phenotype-limited distributions: short-billed birds move away during times that prey bury deeply. R Soc Open Sci 2:150073PubMedPubMedCentralCrossRefGoogle Scholar
  45. Elner RW, Seaman DA (2003) Calidrid conservation: unrequited needs. Wader Study Group Bull 100:30–34Google Scholar
  46. Elner RW, Beninger PG, Jackson DL, Potter TM (2005) Evidence of a new feeding mode in western sandpiper (Calidris mauri) and dunlin (Calidris alpina) based on bill and tongue morphology and ultrastructure. Mar Biol 146:1223–1234CrossRefGoogle Scholar
  47. Engelmoer M, Piersma T, Altenburg W, Mes R (1984) The banc d’Arguin (Mauritania). In: Evans PR, Goss-Custard JD, Hale WG (eds) Coastal waders and wildfowl in winter. Cambridge University Press, Cambridge, pp 293–310Google Scholar
  48. Escudero G, Navedo JG, Piersma T, De Goeij P, Edelaar PIM (2012) Foraging conditions ‘at the end of the world’ in the context of long-distance migration and population declines in red knots. Austral Ecol 37:355–364CrossRefGoogle Scholar
  49. Evans PR, Herdson DM, Knights PJ, Pienkowski MW (1979) Short-term effects of reclamation of part of Seal Sands, Teesmouth, on wintering waders and shelduck. Oecologia 41:183–206PubMedCrossRefPubMedCentralGoogle Scholar
  50. Fenchel TM, Riedl RJ (1970) The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar Biol 7:255–268CrossRefGoogle Scholar
  51. Feng L-H, Ma Y-J (2012) Evolution of tidal flats in China and ecological exploitation of tidal flat resources. Environ Earth Sci 67:1639–1649CrossRefGoogle Scholar
  52. Fisher MR, Hand SC (1984) Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biol Bull 167:445–459PubMedCrossRefPubMedCentralGoogle Scholar
  53. Folmer EO, Piersma T (2012) The contributions of resource availability and social forces to foraging distributions: a spatial lag modelling approach. Anim Behav 84:1371–1380CrossRefGoogle Scholar
  54. Folmer EO, Olff H, Piersma T (2012) The spatial distribution of flocking foragers: disentangling the effects of food availability, interference and conspecific attraction by means of spatial autoregressive modeling. Oikos 121:551–561CrossRefGoogle Scholar
  55. Fuller RA, Bearhop S, Metcalfe NB, Piersma T (2013) The effect of group size on vigilance in ruddy turnstones Arenaria interpres varies with foraging habitat. Ibis 155:246–257CrossRefGoogle Scholar
  56. Furness RW (1993) Birds as monitors of pollutants. In: Furness RW, Greenwood JJD (eds) Birds as monitors of environmental change. Springer, Amsterdam, pp 86–143CrossRefGoogle Scholar
  57. Galbraith H, Jones R, Park R, Clough J, Herrod-Julius S, Harrington B, Page G (2002) Global climate change and sea level rise: potential losses of intertidal habitat for shorebirds. Waterbirds 25:173–183CrossRefGoogle Scholar
  58. Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS One 10:23Google Scholar
  59. Gerritsen AFC, Meiboom A (1986) The role of touch in prey density estimation by Calidris alba. Neth J Zool 36:530–562CrossRefGoogle Scholar
  60. Gill RE Jr, Tibbitts TL, Douglas DC, Handel CM, Malcahy DM, Gottschalck JC, Warnock N, McCaffery BJ, Battley PF, Piersma T (2008) Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc R Soc B 276:447–457CrossRefGoogle Scholar
  61. Gill RE, Canevari P, Iverson EH (1998) Eskimo curlew (Numernius borealisI), version 2.0. In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, IthacaGoogle Scholar
  62. Gratto GW, Thomas MLH, Gratto CL (1984) Some aspects of the foraging ecology of migrant juvenile sandpipers in the outer bay of Fundy. Can J Zool 62:1889–1892CrossRefGoogle Scholar
  63. Guglielmo CG (2010) Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol 50:336–345PubMedCrossRefPubMedCentralGoogle Scholar
  64. Guo Z (1999) Molluscan aquaculture in China. J Shellfish Res 18:19–31Google Scholar
  65. Haramis MG, Link WA, Osenton PC, Carter DB, Weber RG, Clark NA, Teece MA, Mizrahi DS (2007) Stable isotope and pen feeding trial studies confirm the value of horseshoe crab Limulus polyphemus eggs to spring migrant shorebirds in Delaware Bay. J Avian Biol 38:367–376CrossRefGoogle Scholar
  66. Healy T, Wang YX, Healy J (2002) Muddy costs of the world: processes, deposits, and function. Elsevier Science, Amsterdam, 556 pGoogle Scholar
  67. Hemminga MA, Nieuwenhuize J (1991) Transport, deposition and in situ decay of seagrasses in a tropical mudflat area (banc d'Arguin, Mauritania). Neth J Sea Res 27:183–190CrossRefGoogle Scholar
  68. Hicklin PW, Smith PC (1979) The diets of five species of migrant shorebirds in the bay of Fundy. Proc N S Inst Sci 29:483–488Google Scholar
  69. Hicklin PW, Smith PC (1984) Selection of foraging sites and invertebrate prey by migrant semipalmated sandpipers Calidris pusilla (Pallas), in Minas Basin, bay of Fundy. Can J Zool 62:2201–2210CrossRefGoogle Scholar
  70. Hixson SM, Arts MT (2016) Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton. Glob Chang Biol 22:2744–2755PubMedCrossRefPubMedCentralGoogle Scholar
  71. Hixson SM, Sharma B, Kainz MJ, Wacker A, Arts MT (2015) Production, distribution, and abundance of long-chain omega-3 polyunsaturated fatty acids: a fundamental dichotomy between freshwater and terrestrial ecosystems. Environ Rev 23:414–424CrossRefGoogle Scholar
  72. Honkoop PJC, Berghuis EM, Holthuijsen S, Lavaleye MSS, Piersma T (2008) Molluscan assemblages of seagrass-covered and bare intertidal flats on the banc d’Arguin, Mauritania, in relation to characteristics of sediment and organic matter. J Sea Res 60:235–243CrossRefGoogle Scholar
  73. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  74. Iwamura T, Possingham HP, Chadès I, Minton C, Murray NJ, Rogers DI, Treml EA, Fuller RA (2013) Migratory connectivity magnifies the consequences of habitat loss from sea-level rise for shorebird populations. Proc R Soc B 280:20130325PubMedCrossRefPubMedCentralGoogle Scholar
  75. Jardine CB, Bond AL, Davidson PJA, Butler RW, Kuwae T (2015) Biofilm consumption and variable diet composition of western sandpipers (Calidris mauri) during migratory stopover. PLoS One 10:e0124164PubMedPubMedCentralCrossRefGoogle Scholar
  76. Jauffrais T, Drouet S, Turpin V, Meleder V, Jesus B, Cognie B, Raimbault P, Cosson RP, Decottignies P, Martin-Jezequel V (2015) Growth and biochemical composition of a microphytobenthic diatom (Entomoneis paludosa) exposed to shorebird (Calidris alpina) droppings. J Exp Mar Biol Ecol 469:83–92CrossRefGoogle Scholar
  77. Jiménez A, Elner RW, Favaro C, Rickards K, Ydenberg RC (2015) Intertidal biofilm distribution underpins differential tide-following behavior of two sandpiper species (Calidris mauri and Calidris alpina) during northward migration. Estuar Coast Shelf Sci 155:8–16CrossRefGoogle Scholar
  78. Johnsgard PA (1981) The plovers, sandpipers, and snipes of the world. University of Nebraska Press, Lincoln, 519 pGoogle Scholar
  79. Johnson MA, Dioris M, Le Pennec M (1994) Endosymbiotic bacterial contribution in the carbon nutrition of Loripes lucinalis (Mollusca: Bivalvia). Symbiosis 17:1–3Google Scholar
  80. Kalejta B (1993) Intense predation cannot always be detected experimentally: a case study of shorebird predation on nereid polychaetes in South Africa. Neth J Sea Res 31:385–393CrossRefGoogle Scholar
  81. Kennish MJ (2002) Environmental threats and environmental future of estuaries. Environ Conserv 29:78–107CrossRefGoogle Scholar
  82. Koh C-H, Khim JS (2014) The Korean tidal flat of the Yellow Sea: physical setting, ecosystem and management. Ocean Coast Manag 102:398–414CrossRefGoogle Scholar
  83. Kraan C, van Gils JA, Spaans B, Dekinga A, Bijleveld AI, van Roomen M, Kleefstra R, Piersma T (2009) Landscape-scale experiment demonstrates that Wadden Sea intertidal flats are used to capacity by molluscivore migrant shorebirds. J Anim Ecol 78:1259–1268PubMedCrossRefPubMedCentralGoogle Scholar
  84. Kuwae T, Beninger PG, Decottignies P, Mathot KJ, Lund DR, Elner RW (2008) Biofilm grazing in a higher vertebrate: the western sandpiper, Calidris mauri. Ecology 89:599–606PubMedCrossRefPubMedCentralGoogle Scholar
  85. Kuwae T, Miyoshi E, Hosokawa S, Ichimi K, Hosoya J, Amano T, Moriya T, Kondoh M, Ydenberg RC, Elner RW (2012) Variable and complex food web structures revealed by exploring missing trophic links between birds and biofilm. Ecol Lett 15:347–356PubMedCrossRefPubMedCentralGoogle Scholar
  86. Lazarus J, Symonds M (1992) Contrasting effects of protective and obstructive cover on avian vigilance. Anim Behav 43:519–521CrossRefGoogle Scholar
  87. Le Pennec M, Beninger PG, Herry A (1995) Feeding and digestive adaptations of bivalve molluscs to sulphide-rich habitats. Comp Biochem Physiol A 111:183–189CrossRefGoogle Scholar
  88. Leung P, Lee CS, O’Bryen PJ (2008) Species and system selection for sustainable aquaculture. Blackwell, United States Aquaculture Society, 528 pGoogle Scholar
  89. Li X, Li J, Wang Y, Fu L, Fu Y, Li B, Jiao B (2011) Aquaculture industry in China: current state, challenges, and outlook. Rev Fish Sci 19:187–200CrossRefGoogle Scholar
  90. Lin KD, Yuan DX (2005) Degradation kinetics and products of triazophos in intertidal sediment. J Environ Sci 17:933–936Google Scholar
  91. Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809PubMedCrossRefPubMedCentralGoogle Scholar
  92. Lourenço PM, Catry T, Lopes RJ, Piersma T, Granadeiro JP (2017) Invisible trophic links? Quantifying the importance of non-standard food sources for key intertidal avian predators in the eastern Atlantic. Mar Ecol Prog Ser 563:219–232CrossRefGoogle Scholar
  93. MacDonald EC, Ginn MG, Hamilton DJ (2012) Variability in foraging behavior and implications for diet breadth among semipalmated sandpipers staging in the Upper Bay of Fundy. Condor 114:135–144CrossRefGoogle Scholar
  94. Ma ZJ, Melville DS, Liu JG, Chen Y, Yang HY, Ren WW, Zhang ZW, Piersma T, Li B (2014) Rethinking China’s new great wall. Science 346:912–914PubMedCrossRefPubMedCentralGoogle Scholar
  95. MacKinnon J, Verkuil Y, Murray NJ (2012) IUCN situation analysis on east and southeast Asian intertidal habitats, with particular reference to the Yellow Sea (including the Bohai Sea). IUCN, Switzerland, 70 pGoogle Scholar
  96. Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148:547–562CrossRefGoogle Scholar
  97. Martin GR, Piersma T (2009) Vision and touch in relation to foraging and predator detection: insightful contrasts between a plover and a sandpiper. Proc R Soc B 276:437–445PubMedCrossRefPubMedCentralGoogle Scholar
  98. Martini IP, Wanless H (2014) Sedimentary coastal zones from high to low latitudes: similarities and differences (Geological Society of London special publications). The Geological Society, London, 388 p, 600 pGoogle Scholar
  99. Mathot KJ, Elner RW (2004) Evidence for sexual partitioning of foraging mode in western sandpipers (Calidris mauri) during migration. Can J Zool 82:1035–1042CrossRefGoogle Scholar
  100. Mathot KJ, Smith BD, Elner RW (2007) Latitudinal clines in food distribution correlate with differential migration in the western sandpiper. Ecology 88:781–791PubMedCrossRefPubMedCentralGoogle Scholar
  101. Melville DS, Chen Y, Ma Z (2016) Shorebirds along the Yellow Sea coast of China face an uncertain future—a review of threats. Emu 116:100–110CrossRefGoogle Scholar
  102. Moreira F (1995) The winter feeding ecology of avocets, Recurvirostra avosetta, on intertidal areas. I. Feeding strategies. Ibis 137:92–98CrossRefGoogle Scholar
  103. Murray NJ, Fuller RA (2015) Protecting stopover habitat for migratory shorebirds in East Asia. J Ornithol 156:S217–S225CrossRefGoogle Scholar
  104. Murray NJ, Clemens RS, Phinn SR, Possingham HP, Fuller RA (2014) Tracking the rapid loss of tidal wetlands in the Yellow Sea. Front Ecol Environ 12:267–272CrossRefGoogle Scholar
  105. Murray NJ, Ma Z, Fuller RA (2015) Tidal flats of the Yellow Sea: a review of ecosystem status and anthropogenic threats. Aust Ecol 40:472–481CrossRefGoogle Scholar
  106. Myers JP (1986) Sex and gluttony on Delaware Bay. Nat Hist 95:68–77Google Scholar
  107. Niles LJ, Bart J, Sitters HP, Dey AD, Clark KE, Atkinson PW, Baker AJ, Bennett KA, Kalasz KS, Clark NA, Clark J, Gillings S, Gates AS, González PM, Hernandez DE, Minton CDT, Morrison RIG, Porter RR, Ross RK, Veitch CR (2009) Effects of horseshoe crab harvest in Delaware Bay on red knots: are harvest restrictions working? Bioscience 59:153–164CrossRefGoogle Scholar
  108. Oudman T, Bijleveld AI, Kavelaars MM, Dekinga A, Cluderay J, Piersma T, van Gils JA (2016) Diet preferences as the cause of individual differences rather than the consequence. J Anim Ecol 85:1378–1388PubMedCrossRefPubMedCentralGoogle Scholar
  109. Oudman T, Schekkerman H, Kidee A, Roomen MV, Tentij M, Piersma T (2017) The waterbirds of Parc national du banc d’Arguin: evaluation of all complete winter counts, workshop proceedings and an evaluation. Report of programme towards a rich Wadden Sea. NIOZ, Leeuwarden, 23 pGoogle Scholar
  110. Page G, Whitacre DF (1975) Raptor predation on wintering shorebirds. Condor 77:73–83CrossRefGoogle Scholar
  111. Piersma T (1987) Production by intertidal benthic animals and limits to their predation by shorebirds: a heuristic model. Mar Ecol Prog Ser 38:187–196CrossRefGoogle Scholar
  112. Piersma T (2003) Wandernde Kustenvogel im Wattenmeer als Indikatoren globaler Umweltfaktoren. In: Lozan JL, Rachor E, Reise K, Sundermann J, von Westernhagen H (eds) Warnsignale aus Nordsee and Wattenmeer: Eine aktuelle Umweltbilanz. Wissenschaftliche Auswertungen, Hamburg, pp 176–181Google Scholar
  113. Piersma T (2007) Why do molluscivorous shorebirds have such a hard time in the Wadden Sea right now? In: Reineking B, Südbeck P (eds) Seriously declining trends in migratory waterbirds Wadden Sea ecosystem. Common Wadden Sea Secretariat, Wilhemshaven, pp 53–63Google Scholar
  114. Piersma T (2012) What is habitat quality? Dissecting a research portfolio on shorebirds. In: Fuller RJ (ed) Birds and habitat: relationships in a changing landscape. Cambridge University Press, Cambridge, pp 383–407CrossRefGoogle Scholar
  115. Piersma T, Lindström Å (2004) Migrating shorebirds as integrative sentinels of global environmental change. Ibis 146:61–69CrossRefGoogle Scholar
  116. Piersma T, Koolhaas A, Dekinga A (1993) Interactions between stomach structure and diet choice in shorebirds. Auk 110:552–564CrossRefGoogle Scholar
  117. Piersma T, van Aelst R, Kurk K, Berkhoudt H, Maas LRM (1998) A new pressure sensory mechanism for prey detection in birds: the use of principles of seabed dynamics? Proc R Soc B 265:1377–1383CrossRefGoogle Scholar
  118. Piersma T, Koolhaas A, Dekinga A, Beukema JJ, Dekker R, Essink K (2001) Long-term indirect effects of mechanical cockle-dredging on intertidal bivalve stocks in the Wadden Sea. J Appl Ecol 38:976–990CrossRefGoogle Scholar
  119. Piersma T, Rogers DI, González PM, Zwarts L, Niles LJ, De Lima I, Do Nascimento S, Minton CDT, Baker AJ (2005) Fuel storage rates before northward flights in red knots worldwide. In: Greenberg R, Marra PP (eds) Birds of two worlds. Johns Hopkins University Press, Baltimore, pp 262–273Google Scholar
  120. Piersma T, Lok T, Chen Y, Hassell CJ, Yang HY, Boyle A, Slaymaker M, Chan YC, Melville DS, Zhang ZW, Ma Z (2016) Simultaneous declines in summer survival of three shorebird species signals a flyway at risk. J Appl Ecol 53:479–490CrossRefGoogle Scholar
  121. Piersma T, Chang Y-C, Mu T, Hassell CJ, Melville DS, Peng H-B, Ma Z, Zhang Z, Wilcove DS (2017) Loss of habitat leads to loss of birds: reflections on the Jiangsu, China, coastal development plans. Wader Study Group Bull 124:93–98Google Scholar
  122. Pomeroy AC (2006) Tradeoffs between food abundance and predation danger in spatial usage of a stopover site by western sandpipers, Calidris mauri. Oikos 112:629–637CrossRefGoogle Scholar
  123. Pregnall AM, Smith RD, Kursar TA, Alberte RS (1984) Metabolic adaptation of Zostera marina (eelgrass) to diurnal periods of root anoxia. Mar Biol 83:141–147CrossRefGoogle Scholar
  124. Quaintenne G, van Gils JA, Bocher P, Dekinga A, Piersma T (2011) Scaling up ideals to freedom: are densities of red knots across western Europe consistent with ideal free distribution? Proc R Soc B 278:2728–2736PubMedCrossRefPubMedCentralGoogle Scholar
  125. Quinn JL, Cresswell W (2004) Predator hunting behaviour and prey vulnerability. J Anim Ecol 73:143–154CrossRefGoogle Scholar
  126. Quinn JT, Hamilton DJ (2012) Variation in diet of semipalmated sandpipers (Calidris pusilla) during stopover in the upper bay of Fundy, Canada. Can J Zool 90:1181–1190CrossRefGoogle Scholar
  127. Quinn JT, Hamilton DJ, Hebert CE (2017) Fatty acid composition and concentration of alternative prey of semipalmated sandpipers Calidris pusilla in the upper bay of Fundy, Canada. Can J Zool 95:565–573CrossRefGoogle Scholar
  128. R Development Core Team (2017) R: a language and environment for statistical computing. 3.3.3 edn. Vienna, Austria. See
  129. Robin F, Piersma T, Meunier F, Bocher P (2013) Expansion into an herbivorous niche by a customary carnivore: black-tailed godwits feeding on rhizomes of Zostera at a newly established wintering site. Condor 115:340–347CrossRefGoogle Scholar
  130. Rogers DI, Yang H-Y, Hassell CJ, Boyle AN, Rogers KG, Chen B, Zhang Z-W, Piersma T (2010) Red knots (Calidris canutus piersmai and C. c. rogersi) depend on a small threatened staging area in Bohai Bay, China. Emu 110:307–315CrossRefGoogle Scholar
  131. Rubega MA (1997) Surface tension prey transport in shorebirds: how widespread is it? Ibis 139:488–493CrossRefGoogle Scholar
  132. Rubega MA, Obst BS (1993) Surface-tension feeding in phalaropes: discovery of a novel feeding mechanism. Auk 110:169–178Google Scholar
  133. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632CrossRefGoogle Scholar
  134. Saint-Béat B, Dupuy C, Bocher P, Chalumeau J, De Crignis M, Fontaine C, Guizien K, Lavaud J, Lefebvre S, Montanié H, Mouget J-L, Orvain F, Pascal P-Y, Quaintenne G, Radenac G, Richard P, Robin F, Vézina AF, Niquil N (2013) Key features of intertidal food webs that support migratory shorebirds. PLoS One 8:e76739PubMedPubMedCentralCrossRefGoogle Scholar
  135. Sawai Y, Horton BP, Kemp AC, Hawkes AD, Nagumo T, Nelson AR (2016) Relationships between diatoms and tidal environments in Oregon and Washington, USA. Diat Res 31:17–38CrossRefGoogle Scholar
  136. Schneider DC, Harrington B (1981) Timing of shorebird migration in relation to prey depletion. Auk 98:801–811Google Scholar
  137. Shepherd PCF, Boates JS (1999) Effects of a commercial baitworm harvest on semipalmated sandpipers and their prey in the bay of Fundy hemispheric shorebird reserve. Conserv Biol 13:347–356CrossRefGoogle Scholar
  138. Shepherd PCF, Partridge VA, Hicklin PW (1995) Changes in sediment types and invertebrate fauna in the intertidal mudflats of the bay of Fundy between 1977 and 1994. Technical report series 237. Environmental Conservation Branch, Canadian Wildlife Service, Atlantic Region, 49 pGoogle Scholar
  139. Smit J, Piersma T (1989) Numbers, midwinter distribution, and migration of wader populations using the East Atlantic flyway. In: Boyd H, Pirot J-Y (eds) Flyways and reserve networks for water birds. IWRB, Slimbridge, pp 24–63Google Scholar
  140. Spurgeon J (1999) The socio-economic costs and benefits of coastal habitat rehabilitation and creation. Mar Pollut Bull 37:373–382CrossRefGoogle Scholar
  141. St. Clair CT, Baird P, Ydenberg R, Elner R, Bendell LI (2015) Trace elements in Pacific dunlin (Calidris alpina pacifica): patterns of accumulation and concentrations in kidneys and feathers. Ecotoxicology 24:29–44PubMedCrossRefPubMedCentralGoogle Scholar
  142. Stal LJ (2003) Microphytobenthos, their extracellular polymeric substances, and the morphogenesis of intertidal sediments. Geomicrobiol J 20:463–478CrossRefGoogle Scholar
  143. Stonik V, Stonik I (2015) Low-molecular-weight metabolites from diatoms: structures, biological roles and biosynthesis. Mar Drugs 13:3672–3709PubMedPubMedCentralCrossRefGoogle Scholar
  144. Struyf E, Van Damme S, Meire P (2004) Possible effects of climate change on estuarine nutrient fluxes: a case study in the highly nutrified Schelde estuary (Belgium, the Netherlands). Estuar Coast Shelf Sci 60:649–661CrossRefGoogle Scholar
  145. Studds CE, Kendall BE, Murray NJ, Wilson HB, Rogers DI, Clemens RS, Gosbell K, Hassell CJ, Jessop R, Melville DS, Milton DA, Minton CDT, Possingham HP, Riegen AC, Straw P, Woehler EJ, Fuller RA (2017) Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites. Nat Commun 8:14895PubMedPubMedCentralCrossRefGoogle Scholar
  146. Sutherland TF, Shepherd PCF, Elner RW (2000) Predation on meiofaunal and macrofaunal invertebrates by western sandpipers (Calidris mauri): evidence for dual foraging modes. Mar Biol 137:983–993CrossRefGoogle Scholar
  147. Sutherland TF, Elner RW, O’Neill JD (2013) Roberts Bank: ecological crucible of the Fraser River estuary. Prog Oceanogr 115:171–180CrossRefGoogle Scholar
  148. Tang B, Zhang D, Ge B, Zhang H (2013) Sustainable utilization of biological resources from coastal wetlands in China. China Sci Bull 58:2270–2275CrossRefGoogle Scholar
  149. Taylor CM, Laughlin AJ, Hall RJ (2016) The response of migratory populations to phenological change: a migratory flow network modelling approach. J Anim Ecol 85:648–659CrossRefGoogle Scholar
  150. Twining CW, Brenna JT, Hairston NG, Flecker AS (2016) Highly unsaturated fatty acids in nature: what we know and what we need to learn. Oikos 125:749–760CrossRefGoogle Scholar
  151. Underwood GJC, Paterson DM (2003) The importance of extracellular carbohydrate production by marine epipelic diatoms. In: Callow JA (ed) Advances in botanical research, vol 40, pp 183–240CrossRefGoogle Scholar
  152. van de Kam J, Ens B, Piersma T, Zwarts L (2004) Shorebirds: an illustrated behavioural ecology. KNNV, Utrecht, 368 pGoogle Scholar
  153. van de Kam J, Jonkers B, Piersma T (2016) Marathon migrants: celebrating the birds that connect places and people across our planet. Bornmeer, Gorredijk, 208 pGoogle Scholar
  154. van den Hout PJ, van Gils JA, Robin F, van der Geest M, Dekinga A, Piersma T (2014) Interference from adults forces young red knots to forage for longer and in dangerous places. Anim Behav 88:137–146CrossRefGoogle Scholar
  155. van den Hout PJ, Piersma T, ten Horn J, Spaans B, Lok T (2017) Individual shifts toward safety explain age-related foraging distribution in a gregarious shorebird. Behav Ecol 28:419–428Google Scholar
  156. van der Geest M, Sall AA, Ely SO, Nauta RW, van Gils JA, Piersma T (2014) Nutritional and reproductive strategies in a chemosymbiotic bivalve living in a tropical intertidal seagrass bed. Mar Ecol Prog Ser 501:113–126CrossRefGoogle Scholar
  157. van der Heide T, Govers LL, de Fouw J, Olff H, van der Geest M, van Katwijk MM, Piersma T, van de Koppel J, Silliman BR, Smolders AJP, van Gils JA (2012) A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336:1432–1434PubMedCrossRefPubMedCentralGoogle Scholar
  158. van der Meer J, Piersma T, Beukema JJ (2001) Population dynamics of benthic species on tidal flats: the possible roles of shorebird predation. Ecol Stud 151:317–335CrossRefGoogle Scholar
  159. van Gils JA, Dekinga A, Spaans B, Vahl WK, Piersma T (2005) Digestive bottleneck affects foraging decisions in red knots Calidris canutus. II. Patch choice and length of working day. J Anim Ecol 74:120–130CrossRefGoogle Scholar
  160. van Gils JA, van der Geest M, Jansen EJ, Govers LL, de Fouw J, Piersma T (2012) Trophic cascade induced by molluscivore predator alters pore-water biogeochemistry via competitive release of prey. Ecology 93:1143–1152PubMedCrossRefPubMedCentralGoogle Scholar
  161. van Gils JA, van der Geest M, Leyrer J, Oudman T, Lok T, Onrust J, de Fouw J, van der Heide T, van den Hout PJ, Spaans B, Dekinga A, Brugge M, Piersma T (2013) Toxin constraint explains diet choice, survival and population dynamics in a molluscivore shorebird. Proc R Soc B 280:20130861PubMedCrossRefPubMedCentralGoogle Scholar
  162. van Gils JA, Lisovski S, Lok T, Meissner W, Ożarowska A, de Fouw J, Rakhimberdiev E, Soloviev MY, Piersma T, Klaassen M (2016) Body shrinkage due to Arctic warming reduces red knot fitness in tropical wintering range. Science 352:819–821PubMedCrossRefPubMedCentralGoogle Scholar
  163. van Roomen M, Laursen K, van Turnhout C, van Winden E, Blew J, Eskildsen K, Günther K, Hälterlein B, Kleefstra R, Potel P, Schrader S, Luerssen G, Ens BJ (2012) Signals from the Wadden Sea: population declines dominate among waterbirds depending on intertidal mudflats. Ocean Coast Manag 68:79–88CrossRefGoogle Scholar
  164. Vézina F, Williams TD, Piersma T, Morrison RIG (2012) Phenotypic compromises in a long-distance migrant during the transition from migration to reproduction in the high Arctic. Funct Ecol 26:500–512CrossRefGoogle Scholar
  165. Wang Y, Zhang Y (1995) Juvenile mollusk production of marine commercial bottom shell in China. J Fish China 19:166–171Google Scholar
  166. Wang W, Liu H, Li Y, Su J (2014) Development and management of land reclamation in China. Ocean Coast Manag 102:415–425CrossRefGoogle Scholar
  167. Warnock N, Elphick C, Rubega MA (2002) Shorebirds in the marine environment. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC, Washington, pp 581–615Google Scholar
  168. Weber JM (2009) The physiology of long-distance migration: extending the limits of endurance metabolism. J Exp Biol 212:593–597PubMedCrossRefPubMedCentralGoogle Scholar
  169. Weber LM, Haig SM (1997) Shorebird-prey interaction in South Carolina coastal soft sediments. Can J Zool 75:245–252CrossRefGoogle Scholar
  170. Weerman EJ, Herman PMJ, van de Koppel J (2011) Top-down control inhibits spatial self-organization of a patterned landscape. Ecology 92:487–495PubMedPubMedCentralCrossRefGoogle Scholar
  171. Whitlatch RB (1977) Seasonal changes in community structure of macrobenthos inhabiting intertidal sand and mud flats of Barnstable Harbor, Massachusetts. Biol Bull 152:275–294CrossRefGoogle Scholar
  172. Wijnsma G, Wolff WJ, Meijboom A, Duiven P, de Vlas J (1999) Species richness and distribution of benthic tidal flat fauna of the banc d'Arguin, Mauritania. Oceanol Acta 22:233–243CrossRefGoogle Scholar
  173. Wilson WHJ (1990) The relationship between prey abundance and foraging site selection by Semipalmated Sandpipers on a Bay of Fundy mudflat. J Field Ornithol 61:9–19Google Scholar
  174. Wilson WHJ, Vogel ER (1997) The foraging behavior of semipalmated sandpipers in the Upper Bay of Fundy: stereotyped or prey-sensitive? Condor 99:206–210CrossRefGoogle Scholar
  175. Wilson HB, Kendall BE, Fuller RA, Milton DA, Possingham HP (2011) Analyzing variability and the rate of decline of migratory shorebirds in Moreton Bay, Australia. Conserv Biol 25:758–766PubMedCrossRefPubMedCentralGoogle Scholar
  176. Wolff WJ, Duiven AG, Duiven P, Esselink P, Gueye A, Meijboom A, Moerland G, Zegers J (1993) Biomass of macrobenthic tidal flat fauna of the banc d'Arguin, Mauritania. Hydrobiologia 258:151–163CrossRefGoogle Scholar
  177. Yang H-Y, Chen B, Barter M, Piersma T, Zhou C-F, Li F-S, Zhang Z-W (2011) Impacts of tidal land reclamation in Bohai Bay, China: ongoing losses of critical Yellow Sea waterbird staging and wintering sites. Bird Cons Int 21:241–259CrossRefGoogle Scholar
  178. Yang H-Y, Chen B, Ma Z-j, Hua N, van Gils JA, Zhang Z-W, Piersma T (2013) Economic design in a long-distance migrating molluscivore: how fast-fuelling red knots in Bohai Bay, China, get away with small gizzards. J Exp Biol 216:3627–3636PubMedCrossRefPubMedCentralGoogle Scholar
  179. Yang H-Y, Chen B, Piersma T, Zhang Z, Ding C (2016) Molluscs of an intertidal soft-sediment area in China: does overfishing explain a high density but low diversity community that benefits staging shorebirds? J Sea Res 109:20–28CrossRefGoogle Scholar
  180. Ydenberg RC, Butler RW, Lank DB, Guglielmo CG, Lemon M, Wolfe N (2002) Trade-offs, condition dependence and stopover site selection by migrating sandpipers. J Avian Biol 33:47–55CrossRefGoogle Scholar
  181. Zharikov Y, Skilleter GA (2003) Depletion of benthic invertebrates by bar-tailed godwits Limosa lapponica in a subtropical estuary. Mar Ecol Prog Ser 254:151–162CrossRefGoogle Scholar
  182. Zwarts L, Drent RH (1981) Prey depletion and the regulation of predator density: oystercatchers (Haematopus ostralegus) feeding on mussels (Mytilus Edulis). In: Jones NV, Wolff WJ (eds) Feeding and survival srategies of estuarine organisms. Springer US, Boston, pp 193–216CrossRefGoogle Scholar
  183. Zwarts L, Wanink JH (1993) 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. Neth J Sea Res 31:441–476CrossRefGoogle Scholar
  184. Zweers GA, Gerritsen AFC (1997) Transitions from pecking to probing mechanisms in waders. Neth J Zool 47:161–208CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Kimberley J. Mathot
    • 1
    Email author
  • Theunis Piersma
    • 2
    • 3
  • Robert W. Elner
    • 4
  1. 1.Canada Research Chair in Integrative Ecology, Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Department of Coastal SystemsNIOZ Royal Netherlands Institute for Sea Research and Utrecht UniversityTexelThe Netherlands
  3. 3.Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences (GELIFES)University of GroningenGroningenThe Netherlands
  4. 4.Environment and Climate Change Canada, Pacific Wildlife Research CentreDeltaCanada

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