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Relationships Between Sandpipers and Horseshoe Crab in Delaware Bay: A Synthesis

  • David S. Mizrahi
  • Kimberly A. Peters
Chapter

Abstract

Recent and dramatic declines have been documented in several shorebird populations that stage in Delaware Bay during spring migration. As a result, considerable attention has been given to issues such as the reliance of sandpipers on Delaware Bay American horseshoe crab (Limulus polyphemus) eggs for refueling and how to best manage the horseshoe crab fishery to insure adequate resources for migratory shorebirds. In this chapter, we synthesize over 25 years of shorebird research and monitoring data in Delaware Bay to support the premise that horseshoe crab eggs are an essential element for migrating sandpipers during northbound passage through the bay. We then discuss long- and short-term trends in American horseshoe crab populations resulting from changes in demand and harvest regulations, and how this has affected shorebird population viability. Regulatory actions have led to recent increases in some demographic elements of the Delaware Bay crab population, but such changes have not yet translated into increased crab egg availability or population recovery indices in shorebirds. Because reduced availability of horseshoe crab eggs has severe consequences for migratory sandpipers at the individual and population levels, current conservation strategies that include harvest reductions on American horseshoe crabs in the Delaware Bay region must persist into the foreseeable future to insure the recovery of horseshoe crab populations and the long-term health of migratory sandpipers in Delaware Bay.

Keywords

Horseshoe Crab Spring Migration Stopover Site Fuel Deposition Rate Semipalmated Sandpiper 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alerstam T, Hedenström A (1998) The development of bird migration theory. J Avian Biol 29:343–369Google Scholar
  2. Alerstam T, Lindström Å (1990) Optimal bird migration: the relative importance of time, energy, and safety. In Gwinner E (ed) Bird Migration: Physiology and Ecophysiology, Springer, Berlin, pp 331–351Google Scholar
  3. Alerstam T, Gudmundsson GA, Johannesson K (1992) Resources for long distance migration: intertidal exploitation of Littorina and Mytilus by knots Calidris canutus in Iceland. Oikos 65:179–189Google Scholar
  4. [ASMFC] Atlantic States Marine Fisheries Commission (1998) Stock Assessment Report no. 98-01 of the Atlantic States Marine Fisheries Commission. Terms of Reference and Advisory Report for the Horseshoe Crab Stock Assessment Peer Review. ASMFC, Washington, DC 15 ppGoogle Scholar
  5. [ASMFC] Atlantic States Marine Fisheries Commission (2004a) Addendum III to the interstate fishery management plan for horseshoe crab. Fishery Management Report no. 32cGoogle Scholar
  6. [ASMFC] Atlantic States Marine Fisheries Commission (2004b) Horseshoe crab 2004 stock assessment report. February 2004. http://www.asmfc.org/ accessed 7/24/2008
  7. [ASMFC] Atlantic States Marine Fisheries Commission (2006) Addendum IV to the interstate fishery management plan for horseshoe crab. Fishery Management Report no. 32cGoogle Scholar
  8. Atkinson PW, Baker AJ, Bennett KA, Clark NA, Clark JA, Cole KB, Dekinga A, Dey A, Gillings S, Gonzalez PM, Kalasz K, Minton CDT, Newton J, Niles LJ, Piersma T, Robinson RA, and Sitters HJ (2007) Rates of mass gain and energy deposition in red knot on their final spring staging site is both time- and condition-dependent. J Appl Ecol 44:885–895Google Scholar
  9. Bairlein F (1998) The effect of diet composition on migratory fuelling in garden warblers Sylvia borin. J Avian Biol 29:546–551Google Scholar
  10. Bairlein F (1999) Energy and nutrient utilisation efficiencies in birds: a review. In Adams NJ, Slotow RH (eds) Proc 22nd Int Ornithol Congr, Durban, South Africa, pp 2221–2246Google Scholar
  11. Bairlein F, Gwinner E (1994) Nutritional mechanisms and temporal control of migratory energy accumulation in birds. Ann Rev Nutr 14:187–215Google Scholar
  12. Baker RR (1978) The Evolutionary Ecology of Animal Migration. Holmes and Meier, New YorkGoogle Scholar
  13. Baker AJ, González PM, Piersma T, Niles LJ, de Lima Serrano do Nascimento I, Atkinson PW, Clark NA, Minton CDT, Peck M Aarts G (2004) Rapid population decline in Red Knots: fitness consequences of decreased refueling rates and late arrival in Delaware Bay. Proc Roy Soc Lond B Bio 271:875–882Google Scholar
  14. Bart J, Brown S, Harrington B, Morrison RIG (2007) Survey trends of North American shorebirds: population declines or shifting distributions? J Avian Biol 38:73–82Google Scholar
  15. Battley PF, Dietz MW, Piersma, Tang S, Dekinga A, Hulsman K (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc Roy Soc Lond B Bio 267:191–196Google Scholar
  16. Battley PF, Dietz MW, Piersma T, Dekinga A, Tang S, Hulsman K (2001) Is long-distance bird flight equivalent to a high-energy fast? Body composition changes in freely migrating and captive fasting great knots. Physiol Biochem Zool 74: 435–449PubMedGoogle Scholar
  17. Battley PF, Rogers DI, van Gils JA, Piersma T, Hassell CJ, Boyle A, Yang H-Y (2005) How do red knots Calidris canutus leave Northwest Australia in May and reach the breeding grounds in June? Predictions of stopover times, fuelling rates and prey quality in the Yellow Sea. J Avian Biol 36:494–500Google Scholar
  18. Berthold P (1996) Control of Bird Migration. Chapman and Hall, LondonGoogle Scholar
  19. Beukema JJ (1993) Increased mortality in alternative bivalve prey during a period when the tidal flats of the Dutch Wadden Sea were devoid of mussels. Netherlands J Sea Res 31:395–406Google Scholar
  20. Biebach H (1996) Energetics of winter and migratory fattening. In: Carey C (ed) Avian Energetics and Nutritional Ecology. Chapman and Hall, New York, pp 280–323Google Scholar
  21. Biebach H (1998) Phenotypic organ flexibility in Garden Warblers Sylvia borin during long-distance migration. J Avian Biol 29:529–535Google Scholar
  22. Blem CR (1990) Avian energy storage. In: Power DE (ed), Current Ornithology, vol. 7. Plenum, New York, pp 59–114Google Scholar
  23. Botton, ML (1984) Effect of Laughing Gull and shorebird predation on the intertidal fauna at Cape May, NJ. Est Coast Shelf Sci 18:209–220Google Scholar
  24. Botton ML, Harrington BA, Tsipoura N, Mizrahi DS (2003) Synchronies in migration: shorebirds, horseshoe crabs and Delaware Bay. In: Shuster CN Jr, Barlow RB, Brockman HJ (eds) The American Horseshoe Crab. Harvard University Press, Cambridge, pp 5–32Google Scholar
  25. Botton ML, Loveland RE, Jacobsen TR (1988) Beach erosion and geochemical factors influence on spawning success of horseshoe crabs (Limulus polyphemus) in Delaware Bay. Mar Biol 99:325–332Google Scholar
  26. Botton ML, Loveland RE, Jacobsen TR (1994) Site selection by migratory shorebirds in Delaware Bay, and its relationship to beach characteristics and abundance of horseshoe crab eggs Limulus polyphemus eggs. Auk 111:605–616Google Scholar
  27. Boyd H (1992) Arctic summer conditions and British knot numbers: an exploratory analysis. Wader Study Group Bull 64(Suppl):144–152Google Scholar
  28. Boyd H, Piersma T (2001) Changing balance between survival and recruitment explains population trends in red knots Calidris canutus islandica wintering in Britain, 1969–1995. Ardea 89:301–317Google Scholar
  29. Brown S, Hickey C, Harrington B, Gill R (eds) (2001) The U.S. Shorebird Conservation Plan, Second edition. Manomet Center for Conservation Sciences, Manomet, MA, 66 ppGoogle Scholar
  30. Brust J, Davis M, McKown K, Michels S, Millard M, Smith D, Spear B (2006) Review of Horseshoe Crab Population Models. Horseshoe Crab Technical CommitteeGoogle Scholar
  31. Burger J, Carlucci SA, Jeitner CW, Niles L (2007) Habitat choice, disturbance, and management of foraging shorebirds and gulls at a migratory stopover. J Coastal Res 23:1159–1166Google Scholar
  32. Burger J, Niles L, Clark KE (1997) Importance of beach, mudflat and marsh habitats to migrant shorebirds on Delaware Bay. Biol Conserv 79:283–292Google Scholar
  33. Caldow RWG, Goss-Custard JD, Stillman RA, Le V Durrell SEA, Swinfen R, Bregnballe T (1999) Individual variation in the competitive ability of interference-prone foragers: the relative importance of foraging efficiency and susceptibility to interference. J Anim Ecol 68:869–878Google Scholar
  34. Castro G, Myers JP (1988) A statistical method to estimate the cost of flight in birds. J Field Ornithol 59:369–338Google Scholar
  35. Castro G, Myers JP (1993) Shorebird predation on eggs of horseshoe crabs during spring stopover on Delaware Bay. Auk 110:927–930Google Scholar
  36. Castro G, Myers JP Place AR (1989) Assimilation efficiency of Sanderlings (Calidris alba) feeding on horseshoe crab (Limulus polyphemus) eggs. Physiol Zool 62:716–731Google Scholar
  37. Clark KE, Niles LJ Burger J (1993) Abundance and distribution of migrant shorebirds in Delaware Bay. Condor 95:694–705Google Scholar
  38. Cramp S, Simmons KS (eds.) (1983) The Birds of the Western Palearctic, Vol. 3. Oxford University Press, OxfordGoogle Scholar
  39. Davidson NC, Evans PR (1989) Prebreeding accumulation of fat and muscle protein by Arctic-breeding shorebirds. Proc 20th Int Ornithol Congr, 1098–1104Google Scholar
  40. Davis ML, Berkson J, Kelly M (2006) A production modeling approach to the assessment of the horseshoe crab (Limulus polyphemus) population in Delaware Bay. Fish Bull 104:215–225Google Scholar
  41. Dingle H (1996) Migration, the Biology of Life on the Move. Oxford University Press, OxfordGoogle Scholar
  42. Drent R, Both C, Green M, Madsen J, Piersma T (2003) Pay-offs and penalties of competing migratory schedules. Oikos 103:274–292Google Scholar
  43. Escudero G, Niles LJ (2001) Are there alternative food resources for knots in Delaware Bay? Wader Study Group Bull 95:13Google Scholar
  44. Farmer AH, Wiens JA (1999) Models and reality: time-energy trade-offs in Pectoral Sandpiper (Calidris melanotos) migration. Ecology 80:2566–2580Google Scholar
  45. Gauthreaux, Jr SA (1982) The ecology and evolution of avian migration systems. In Farner DS, King JR (eds), Avian biology, Vol. I, Academic Press, New York, pp 93–168Google Scholar
  46. Gillings S, Atkinson PW, Bardsley SL, Clark NA, Love SE, Robinson RA, Stillman RA, Weber RG (2007) Shorebird predation of horseshoe crab eggs in Delaware Bay: species contrasts and availability constraints. J Anim Ecol 76:503–514PubMedGoogle Scholar
  47. Gonzalez PM, Baker A, Minton C, Niles L, Carter D, Clark N (2001) Migratory fattening of red knots in Delaware Bay, 1997–2000. Wader Study Group Bull 95:12–13Google Scholar
  48. Goss-Custard JD, Stillman RA, West AD, Caldow RWG, Triplet P, le V dit Durell SEA, McGrorty S (2003) When enough is not enough: shorebirds and shellfishing. Proc Roy Soc Lond B Biol 271:233–237Google Scholar
  49. Gudmundsson GA, Lindström Å, Alerstam T (1991) Optimal fat loads and long-distance flights by migrating Knots Calidris canutus, Sanderlings C. alba and Turnstones Arenaria interpres. Ibis 133:140–152Google Scholar
  50. Haramis GM, Link WA, Osenton PC, Carter DB, Weber RG, Clark NA, Teese MA, Mizrahi DS (2007) Stable isotope and pen feeding studies confirm the value of horseshoe crab (Limulus polyphemus) eggs to spring migrant shorebirds in Delaware Bay. J Avian Biol 38:367–376Google Scholar
  51. Hata D (2008) Report of the 2007 Horseshoe crab spawning activity in Delaware Bay: 1999–2007. Report to the ASMFC Horseshoe Crab Technical CommitteeGoogle Scholar
  52. Hata D, Berkson J (2003) Abundance of horseshoe crabs (Limulus polyphemus) in the Delaware Bay area. Fish Bull 101:933–938Google Scholar
  53. Hedenström A, Alerstam T (1997) Optimum fuel loads in migratory birds: distinguishing between time and energy minimization. J Theor Biol 189:227–234PubMedGoogle Scholar
  54. Hedenström A, Alerstam T (1998) How fast can birds migrate? J Avian Biol 29:424–432Google Scholar
  55. Hitchcock CL, Gratto-Trevor C (1997) Diagnosing a shorebird local population decline with a stage-structured population model. Ecology 78:522–534Google Scholar
  56. Howe MA, Geissler J, Harrington BA (1989) Population trends of North American shorebirds based on the International Shorebird Survey. Biol Conserv 49:185–199Google Scholar
  57. Jackson NL, Nordstrom KF, Smith DR (2002) Geomorphic-biotic interactions on beach foreshores in estuaries. J Coastal Res 36:414–424Google Scholar
  58. Jehl, Jr JR (1997) Cyclical changes in body composition in the annual cycle and migration of the Eared Grebe, Podiceps nigricollis. J Avian Biol 28:132–142Google Scholar
  59. Jehl, Jr JR (2007) Disappearance of breeding semipalmated sandpipers from Churchill, Manitoba: more than a local phenomenon. Condor 109:351–360Google Scholar
  60. Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol. 29: 521–528Google Scholar
  61. Jenni-Eiermann S, Jenni L (1994) Plasma metabolite levels predict individual: body-mass changes in a small long-distance migrant, the garden warbler. Auk 111:888–899Google Scholar
  62. Jenni-Eiermann S, Jenni L (2003) Fuel deposition rates in migrating birds: causes, constraints and consequences. In: Berthold P, Gwinner E, Sonneneschein E (eds), Avian Migration. Springer-Verlag, New York, pp.293–306Google Scholar
  63. Jenni-Eiermann S, Jenni L, Kvist A, Lindström Å, Piersma T, Visser HG (2002) Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205: 2453–2460PubMedGoogle Scholar
  64. Kalasz K, Hernandez D, Dey A (2008) Delaware Bay egg survey: 2005–2007. Report to the United States Fish and Wildlife Service’s Shorebird Technical Committee U.S. Fish and Wildlife Service, Division of Migratory Bird Management, Arlington, VA, 19 ppGoogle Scholar
  65. Karpanty SH, Fraser JD, Berkson J, Niles LJ, Dey A, Smith EP (2006) Horseshoe crab eggs determine red knot distribution in Delaware Bay. J Wildlife Manage 70:1704–1710Google Scholar
  66. Kreamer G, Michels S (2008) History of horseshoe crab harvest on Delaware Bay. In: Tanacredi JT, Botton, ML, Smith DR (eds), Biology and Conservation of Horseshoe Crabs. Springer, New YorkGoogle Scholar
  67. Kersten M, Piersma T (1987) High levels of energy expenditure in shorebirds: metabolic adaptations to an energetically expensive way of life. Ardea 75:175–187Google Scholar
  68. Kvist A, Lindström Å (2003) Gluttony in migratory waders – unprecedented energy assimilation rates in vertebrates. Oikos 103:397–402Google Scholar
  69. Kvist A, Lindström Å, Green M, Piersma T, Visser HG (2001) Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413:730–732PubMedGoogle Scholar
  70. Lindström Å, Alerstam T (1992) Optimal fat loads in migrating birds: a test of the time-minimization hypothesis. Am Nat 140:477–491PubMedGoogle Scholar
  71. Lyons JE, Collazo JA, Guglielmo CG (2008) Plasma metabolites and migration physiology of semipalmated sandpipers: refueling performance at five latitudes. Oecologia 155:417–427Google Scholar
  72. McGowan A, Cresswell W, Ruxton GD (2002) The effects of daily weather variation on foraging and responsiveness to disturbance in overwintering red knot Calidris canutus. Ardea 90: 229–237Google Scholar
  73. McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393Google Scholar
  74. Michels S, Smith D, Bennett S (2008) Horseshoe crab spawning activity in Delaware Bay: 1999–2007. Report to the ASMFC Horseshoe Crab Technical Committee, 17 ppGoogle Scholar
  75. Mizrahi DS (1999) Migratory behavior and ecophysiology of Semipalmated Sandpipers during spring migration stopover. PhD dissertation, Clemson University, Clemson, South Carolina.Google Scholar
  76. Moore FR, Gauthreaux, Jr SA, Kerlinger P, Simons TR (1993) Stopover habitat: management implications and guidelines. In: Finch D, Stangel P (eds), Status and Management of Neotropical Birds. Rocky Mountain Forest and Range Experimental Station, U.S. Department .of Agriculture, Fort Collins, CO, pp 58–69Google Scholar
  77. Moore FR, Gauthreaux, Jr SA, Kerlinger P, Simons TR (1995) Habitat requirements during migration: important link to conservation. In: Martin TE, Finch DM, (eds), Ecology and Management of Neotropical Migratory Birds. Oxford University Press, New York, pp 121–144Google Scholar
  78. Morrison RIG (1984) Migration systems of some New World shorebirds. In: Burger J, Olla BL, (eds), Behavior of Marine Animals, vol. 6, Shorebirds: Migration and Foraging Behavior. Plenum Press, New York, pp 125–202Google Scholar
  79. Morrison RIG, Hobson KA (2004) Use of body stores in shorebirds after arrival on high-Arctic breeding grounds. Auk 121:333–344Google Scholar
  80. Morrison RIG, Ross RK (1989) Atlas of Nearctic Shorebirds on the Coast of South America. Canadian Wildlife Service Special Publication, Ottawa.Google Scholar
  81. Morrison RIG, Aubry Y, Butler RW, Beyersbergen GW, Donaldson GM, Gratto-Trevor CL, Hicklin PW, Johnston VH, Ross RK (2001) Declines in North American shorebird populations. Wader Study Group Bull 94:34–38Google Scholar
  82. Morrison RIG, Ross RK, Niles LJ (2004) Declines in wintering populations of Red Knots in southern South America. Condor 106:60–70Google Scholar
  83. Morrison RIG, Davidson NC, Piersma T (2005) Transformations at high latitudes: why do red knots bring body stores to the breeding grounds? Condor 107:449–457Google Scholar
  84. Morrison RIG, McCaffery BJ, Gill RE, Skagen SK, Jones SL, Page GW, Gratto-Trevor CL, Andres BA (2006) Population estimates of North American shorebirds. Wader Study Group Bull 111:67–85Google Scholar
  85. Morrison RIG, Baker AJ, Gonzalez PM, Niles LJ, Ross RK (2007) Status Report on the Red Knot Calidris canutus. Report prepared for the Committee on the Status of Endangered Wildlife in Canada [COSEWIC]. http://www.gov.ns.ca/natr/wildlife/BIODIV/species_recovery/statusreports/sr_RedKnotDraft.pdf, accessed 8 May 2008
  86. Myers JP (1983) Conservation of migrating shorebirds: Staging areas, geographic bottlenecks and regional movements. Am Birds 37:23–24Google Scholar
  87. Myers JP (1986) Sex and gluttony on Delaware Bay. Nat Hist 95:68–77Google Scholar
  88. Myers JP, Morrison RIG, Antas PZ, Harrington BA, Lovejoy TE, Sallaberry M, Senner SE, Tarak A (1987) Conservation strategy for migratory species. Am Sci 75:19–26Google Scholar
  89. Niles L, Clark K, Minton C, Clark N, Baker A, Sitters H (2001) Trends in mass and numbers of red knots, ruddy turnstones and sanderlings on the Delaware Bay, USA. Wader Study Group Bull 95:10Google Scholar
  90. Niles LJ, Sitters HP, Dey AD, Baker AJ, Morrison RIG, Hernandez D, Clark KE, Harrington BA, Peck MK, Gonzalez PM, Bennett KA, Kalasz K, Atkinson PW, Clark NA, Minton CDT (2007) Status of the Red Knot (Calidris canutus rufa) in the Western Hemisphere. US Fish Wildlife Service, New Jersey, USA, http://www.audubon.org/campaign/esa/doc/red_knot_report.pdf, accessed 8 May, 2008
  91. Nordstrom K, Jackson N, Smith D, Weber R (2006) Transport of horseshoe crab eggs by waves and swash on an estuarine beach: Implications for foraging shorebirds. Est Coast Shelf Sci 70:438–448Google Scholar
  92. Odell J, Mather ME, Muth RM (2005) A biosocial approach for analyzing environmental conflicts: a case study of horseshoe crab allocation. BioScience 55:735–748Google Scholar
  93. Pfister C, Harrington BA, Lavine M (1992) The impact of human disturbance on shorebirds at a migration staging area. Biol Conserv 60:115–126Google Scholar
  94. Pfister C, Kasprzyk MJ, Harrington BA (1998) Body fat levels and annual return in migrating Semipalmated Sandpipers. Auk 115:904–915Google Scholar
  95. Pierce BJ, McWilliams SR (2005) Seasonal changes in composition of lipid stores in migratory birds: causes and consequences. Condor 107:269–279Google Scholar
  96. Piersma, T. 1990. Premigratory fattening usually involves more than the deposition of fat alone. Ring Migrat 11:113–115Google Scholar
  97. Piersma T (1998) Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight. J Avian Biol 29:511–520Google Scholar
  98. Piersma T, Baker AJ (2000) Life history characteristics and the conservation of migratory shorebirds. In: Gosling LM, Sutherland WJ (eds), Behaviour and Conservation. Cambridge University Press, London, pp 105–124Google Scholar
  99. Piersma T, Davidson N (1992) The migration of knots. Wader Study Group Bull 64 (suppl), 209 ppGoogle Scholar
  100. Piersma T, Gill Jr, RE (1998) Guts don't fly: small digestive organs in obese Bar-tailed Godwits. Auk 115:196–203Google Scholar
  101. Piersma T, Jukema J (1990) Budgeting the flight of a long-distance migrant: changes in nutrient reserve levels of bar-tailed godwits at successive spring staging sites. Ardea 78:315–337Google Scholar
  102. Piersma T, Lindström Å (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138PubMedGoogle Scholar
  103. Piersma T, Hoekstra R, Dekinga A, Koolhaas A, Wolf P, Battley P, Wiersma P (1993) Scale and intensity of intertidal habitat use by knots Calidris canutus in the western Wadden Sea in relation to food, friends and foes. Netherlands J Sea Res 31:331–357Google Scholar
  104. Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415PubMedGoogle Scholar
  105. Piersma T, Rogers DI, Gonzalez PM, Zwarts L, Niles LJ, de Lima Serrano do Nascimento I, Minton CDT, Baker AJ (2005) Fuel storage rates before northward flights in red knots worldwide: facing the severest ecological constraint in tropical intertidal environments? In: Greenberg R, Marra PP, (eds), Birds of Two Worlds: Ecology and Evolution of Migration. Johns Hopkins University Press, Baltimore, pp 262–273Google Scholar
  106. Pooler PS, Smith DR, Loveland RE, Botton ML, Michels SF (2003) Assessment of sampling methods to estimate horseshoe crab (Limulus polyphemus) egg density in Delaware Bay. Fish Bull 101:698–703Google Scholar
  107. Ramenofsky M (1990) Fat storage and fat metabolism in relation to migration. In: Gwinner E (ed), Bird Migration: Physiology and Ecophysiology. Springer-Verlag, New York, pp 214–231Google Scholar
  108. Robinson RA, Atkinson PW, Clark, NA (2003) Arrival and weight gain of Red Knots, Ruddy Turnstones and Sanderlings staging in Delaware Bay in spring. Brit Trust Ornith Res Rep No. 307, Thetford, Norfolk, UK, 55 ppGoogle Scholar
  109. Senner SE, Howe MA (1984) Conservation of nearctic shorebirds. In: Burger J, Olla BL (eds), Behavior of Marine Animals, Vol. 5, Shorebirds: Populations and Breeding Behavior. Plenum Press, New York, pp 379–421Google Scholar
  110. Shuster, Jr CN, Botton ML (1985) A contribution to the population biology of horseshoe crabs, Limulus polyphemus (L.), in Delaware Bay. Estuaries 8:363–372Google Scholar
  111. Shuster, Jr CN, Sekiguchi K (2003) Growing up takes about ten years and eighteen stages. In: Shuster CN, Barlow RB, Brockman HJ (eds) The American Horseshoe Crab. Harvard University Press, Cambridge, pp 103–132Google Scholar
  112. Sitters H, Dey A, Niles L, Kalasz K (2005) Day and night feeding and roosting by red knots in Delaware Bay. Wader Study Group Bull 108:21Google Scholar
  113. Skagen SK (2006). Migration stopovers and the conservation of Arctic-breeding calidridine sandpipers. Auk 123:313–322Google Scholar
  114. Skagen, SK, Oman HD (1996) Dietary flexibility of shorebirds in the Western Hemisphere. Can Field Nat 110:419–444Google Scholar
  115. Smith DR (2007) Effect of horseshoe crab spawning density on nest disturbance and exhumation of eggs: a simulation study. Estuar Coasts 30:287–295. Fisheries Commission, Washington DC. Website: http://www.lsc.usgs.gov/aeb/2065/isa%20report%2005.pdf accessed on October 2005Google Scholar
  116. Smith DR., Michels. SF (2006) Seeing the elephant: importance of spatial and temporal coverage in a large-scale volunteer-based program to monitor horseshoe crabs. Fisheries 31:485–491Google Scholar
  117. Smith DR, Pooler PS, Loveland RE, Botton ML, Michels SF, Weber RG, Carter DB (2002a) Horseshoe crab (Limulus polyphemus) reproductive activity on Delaware Bay beaches: interactions with beach characteristics. J Coast Res 18:730–740Google Scholar
  118. Smith DR, Pooler PS, Swan BL, Michels S, Hall WR, Himchak P, Millard MJ (2002b) Spatial and temporal distribution of horseshoe crab (Limulus polyphemus) spawning in Delaware Bay: implications for monitoring. Estuaries 25:115–125Google Scholar
  119. Smith DR, Millard MJ, Eyler S (2006) Abundance of adult horseshoe crabs (Limulus polyphemus) in Delaware Bay estimated from a bay-wide mark-recapture study. Fish Bull 104:456–464Google Scholar
  120. Smith DR, Millard, MJ, Carmichael RH (2008) Comparative status and assessment of Limulus polyphemus with emphasis on the New England and Delaware Bay populations. In: Tanacredi JT, Botton, ML, Smith DR (eds), Biology and Conservation of Horseshoe Crabs. Springer, New YorkGoogle Scholar
  121. Stiles EW (1993) The influence of pulp lipids on fruit preference by birds. Plant Ecol 107/108:227–235Google Scholar
  122. Stillman RA, Poole AE, Goss-Custard JD, Caldow RWG, Yates MG, Triplet P. (2002) Predicting the strength of interference more quickly using behavior-based models. J Anim Ecol 71:532–541Google Scholar
  123. Stillman RA, Atkinson PW, Clark NA, Gillings S, Henderson IG, Love SE, Robinson RA, Weber RG, Bardsley SL (2003) Functional responses of shorebirds feeding on horseshoe crab eggs. Brit Trust Ornith Res Rep No. 308, Norfolk, UK, 41 ppGoogle Scholar
  124. Terborgh J (1992) Perspectives on the conservation of Neotropical migrant landbirds. In: Hagan III, JM, Johnston DW, (eds), Ecology and Conservation of Neotropical Migrant Landbirds. Smithsonian Institution Press, Washington, DC, pp 7–12Google Scholar
  125. Thomas K, Kvitek RG, Bretz C (2003) Effects of human activity on the foraging behavior of sanderlings Calidris alba. Biol Conserv 109:67–71Google Scholar
  126. Triplet P, Stillman RA, Goss-Custard JD (1999) Prey abundance and the strength of interference in a foraging shorebird. J Anim Ecol 68:254–265Google Scholar
  127. Tsipoura N, Burger J (1999) Shorebird diet during spring migration stopover on Delaware Bay. Condor 101:635–644.Google Scholar
  128. USFWS-Shorebird Technical Committee (2003) Delaware Bay shorebird-horseshoe crab assessment report: biological assessment. Andres BA (ed), U.S. Fish and Wildlife Service, Division of Migratory Bird Management, Arlington, VAGoogle Scholar
  129. van Gils JA (2004) Foraging decisions in a digestively constrained long-distance migrant, the red knot (Calidris canutus). PhD Thesis, University of Groningen, Groningen, The NetherlandsGoogle Scholar
  130. van Gils JA, Piersma T, Dekinga A, Dietz MW (2003) Cost-benefit analysis of mollusc-eating in a shorebird. II. Optimizing gizzard size in the face of seasonal demands. J Exp Biol 206:3369–3380PubMedGoogle Scholar
  131. van Gils JA, de Rooij SR, van Belle J, van der Meer J, Dekinga A, Piersma T, Drent R (2005) Digestive bottleneck affects foraging decisions in red knots Calidris canutus. I. Prey choice. J Anim Ecol 74:105–119Google Scholar
  132. van Gils JA, Piersma T, Dekinga A, Spaans B, Kraan C (2006) Shellfish dredging pushes a flexible avian top predator out of a marine protected area. PLoS (Public Library of Science) Biology, 4:e376, http://biology.plosjournals.org/archive/15457885/4/12/pdf/10.1371_journal.pbio.0040376-L.pdf
  133. Wander W, Dunne P (1981) Species and numbers of shorebirds on the Delaware Bay shore of New Jersey, spring 1981. Occasional Paper #140, New Jersey Audubon Society. Rec NJ Birds 7:59–64Google Scholar
  134. Wilcove DS (2008) No Way Home: The Decline of the World's Great Animal Migrations. Island Press, Washington, DCGoogle Scholar
  135. Wilson JR, Barter MA (1998) Identification of potentially important staging areas for “long jump” migrant waders in the east Asian-Australasian flyway during northward migration. Stilt 32:16–28Google Scholar
  136. Zwarts L (1990) Increased prey availability drives premigration hyperphagia in Whimbrels and allows them to leave the Banc D’Arguin, Mauritania, in time. Ardea 78:279–300Google Scholar
  137. Zwarts L, Drent RH (1981) Prey depletion and the regulation of prey density: oystercatchers (Haematopus ostralegus) feeding on mussels (Mytilus edulis). In: Jones NV, Wolff WJ (eds), Feeding and Survival Strategies of Estuarine Organisms. Plenum, New York, pp 193–216Google Scholar
  138. Zwarts L, Ens BJ, Kersten M, Piersma T (1990) Moult, mass and flight range of waders ready to take off for long-distance migrations. Ardea 78:339–364Google Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.New Jersey Audubon Society, Center for Research and EducationCape May Court HouseUSA

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