Stable isotope and pen feeding trial studies confirm the value of horseshoe crab Limulus polyphemus eggs to spring migrant shorebirds in Delaware Bay

Journal of Avian Biology

Volumn 38, Issue 3, 2007, Pages 367-376

  Haramis, G Michael ^a   Link, William A ^a   Osenton, Peter C ^a   Carter, David B ^b   Weber, Richard G ^c   Clark, Nigel A ^d   Teece, Mark A ^e   Mizrahi, David S ^f  

^a PATUXENT WILDLIFE RESEARCH CENTER   (United States)

^b Delaware Department of Natural Resources and Environmental Control   (United States)

^c Delaware National Estuarine Research Reserve   (United States)

^d THE NUNNERY   (United Kingdom)

^e STATE UNIVERSITY OF NEW YORK   (United States)

^f New Jersey Audubon Society   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY MASS; CRAB; EGG; MIGRATORY POPULATION; MOLLUSC; STABLE ISOTOPE; STOPOVER; WADER;

DELAWARE BAY; NORTH AMERICA; UNITED STATES;

ARENARIA (AVES); ARENARIA INTERPRES; ARENARIA INTERPRES MORINELLA; AVES; BIVALVIA; CALIDRIS CANUTUS; CALIDRIS CANUTUS RUFA; DECAPODA (CRUSTACEA); DONAX VARIABILIS; LIMULUS; LIMULUS POLYPHEMUS; MEROSTOMATA; MYTILUS EDULIS;

EID: 34247844361     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.0908-8857.2007.03898.x     Document Type: Article

References (54)

1. Alerstam, T., Gudmundsson, G. A. Johannesson, K. 1992. Resources for long distance migration: intertidal exploitation of Littorina and Mytilus by knots Calidriscanutus in Iceland Oikos 65: 179 189.
2. Atkinson, P. W., Baker, A. J., Bevan, R. M., Clark, N. A., Cole, K. B., Gonzalez, P. M., Newton, J., Niles, L. J. Robinson, R. A. 2005. Unraveling the migration and moult strategies of a long-distance migrant using stable isotopes: red knot Calidris canutus movements in the Americas Ibis 147: 738 749.
3. Baker, A. J., Gonzalez, P. M., Piersma, T., Niles, L. J., de Lima Sarrano do Nascimento, I., Atkinson, P. W., Clark, N. A., Minton, C. D. T., Peck, M. K. Aarts, G. 2004. Rapid population decline in red knots: fitness consequences of decreased refueling rates and late arrival in Delaware Bay Proc. R. Soc. B 271: 875 882.
4. Baker, A. J., Gonzalez, P. M., Serrano, I. L., Junior, W. R. T., Efe, M. A., Rice, S., D'Amico, V. L., Rocha, M. C. Echave, M. E. 2005. Assessment of the wintering area of red knots in Maranhao, northern Brazil in February 2005 Wader Study Group Bull. 107: 10 18.
5. Battley, P. F., Dietz, M. W., Piersma, T., Tang, S., Dekinga, A. Hulsman, K. 2000. Empirical evidence of differential organ reductions during trans-oceanic bird flight Proc. R. Soc. B 267: 191 195.
6. Battley, P. F., Rogers, D. I., van Gils, J. A., Piersma, T., Hassell, C. J., Boyle, A. Hong-Yan, 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: 494 500.
7. Berkson, J. Shuster, C. N., Jr. 1999. The horseshoe crab: the battle for a true multiple-use resource Fisheries 24: 6 11.
8. Botton, M. L. 1984. Effects of laughing gull and shorebird predation on the intertidal fauna at Cape May, New Jersey Est. Coast. Shelf Sci. 18: 209 220.
9. Botton, M. L., Loveland, R. E. Jacobsen, T. R. 1994. Site selection by migratory shorebirds in Delaware Bay, and its relationship to beach characteristics and abundance of horseshoe crab (Limulus polyphemus) eggs Auk 111: 605 616.
10. Burger, J., Niles, L. Clark, K. E. 1997. Importance of beach, mudflat and marsh habitats to migrant shorebirds on Delaware Bay Biol. Cons. 79: 283 292.
11. Castro, G. Myers, J. P. 1993. Shorebird predation on eggs of horseshoe crabs during spring stopover on Delaware Bay Auk 110: 927 930.
12. Clark, K. E., Niles, L. J. Burger, J. 1993. Abundance and distribution of migrant shorebirds in Delaware Bay Condor 95: 694 705.
13. Dekinga, A. Piersma, T. 1993. Reconstructing diet composition on the basis of faeces in a mollusc-eating wader, the knot Calidris canutus Bird Study 40: 144 156.
14. Escudero, G. Niles, L. J. 2001. Are there alternative food resources for knots in Delaware Bay? Wader Study Group Bull. 95: 13.
15. Gannes, L. Z., del Rio, C. M. Koch, P. 1998. Natural abundance variations in stable isotopes and their potential use in animal physiological ecology Comp. Biochem. Physiol. 119A: 725 737.
16. Gonzalez, P. M., Piersma, T. Verkuil, Y. 1996. Food, feeding, and refuelling of red knots during northward migration at San Antonio Oeste, Rio Negro, Argentina J. Field Ornith. 67: 575 591.
17. Gonzalez, P. M., 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 13.
18. Harrington, B. A. 2001. Red knot (Calidris canutus) Poole, A. Gill, F. The birds of North America, No. 563. The birds of North America, Inc., Philadelphia.
19. Hobson, K. A. Clark, R. G. 1992. Assessing avian diets using stable isotope analysis. I. Turnover of carbon-13 Condor 94: 181 188.
20. Hobson, K. A. Clark, R. G. 1993. Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies Auk 110: 638 641.
21. Jenni, L. Jenni-Eiermann, S. 1998. Fuel supply and metabolic constraints in migrating birds J. Avian Biol. 29: 521 528.
22. Jenni-Eiermann, S., Jenni, L., Kvist, A., Lindström, A., Piersma, T. Visser, H. G. 2002. Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird J. Exp. Biol. 205: 2453 2460.
23. Karpanty, S. M., Fraser, J. D., Berkson, J., Niles, L. J., Dey, A. Smith, E. P. 2006. Horseshoe crab eggs determine red knot distribution in Delaware Bay J. Wildl. Manage. 70: 1704 1710.
24. Kelly, J. F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology Can. J. Zool. 78: 1 27.
25. Klaassen, M., Lindström, A., Meltofte, H. Piersma, T. 2001. Arctic waders are not capital breeders Nature 413: 794.
26. Magdych, W. P. 1981. An efficient, inexpensive elutriator design for separating benthos from sediment samples Hydrobiologia. 85: 157 159.
27. McWilliams, S. R., 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: 377 393.
28. Morrison, R. I. G. Harrington, B. A. 1992. The migration system of the red knot Calidris canutus rufa in the New World Wader Study Group Bull. 64 (Suppl.): 71 84.
29. Morrison, R. I. G. Hobson, K. A. 2004. Use of body stores in shorebirds after arrival on high-Arctic breeding grounds Auk 121: 333 344.
30. Morrison, R. I. G., Aubry, Y., Butler, R. W., Beyersbergen, G. W., Donaldson, G. M., Gratto-Trevor, C. L., Hicklin, P. W., Johnston, V. H. Ross, R. K. 2001. Declines in North American shorebird populations Wader Study Group Bull. 94: 34 38.
31. Morrison, R. I. G., Davidson, N. C. Piersma, T. 2005. Transformations at high latitudes: why do red knots bring body stores to the breeding grounds? Condor 107: 449 457.
32. Morrison, R. I. G., Ross, R. K. Niles, L. J. 2004. Declines in wintering populations of red knots in southern South America Condor 106: 60 70.
33. Myers, J. P. 1986. Sex and gluttony on Delaware Bay Nat. Hist. 95: 68 77.
34. Myers, J. P., Morrison, R. I. G., Antas, P. Z., Harrington, B. A., Lovejoy, T. E., Sallaberry, M., Senner, S. E. Tarak, A. 1987. Conservation strategy for migratory species Am. Sci. 75: 18 26.
35. 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: 10.
36. Peterson, B. J. Fry, B. 1987. Stable isotopes in ecosystem studies Ann. Rev. Ecol. Sys. 18: 293 320.
37. Pierce, B. J. McWilliams, S. R. 2005. Seasonal changes in composition of lipid stores in migratory birds: causes and consequences Condor 107: 269 279.
38. Pierce, B. J., McWilliams, S. R., Place, A. R. Huguenin, M. A. 2004. Diet preference for specific fatty acids and their effect on composition of fat reserves in migratory red-eyed vireos (Vireo olivaceous) Comp. Biochem. Physiol. 138A: 503 514.
39. 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: 511 520.
40. Piersma, T. Baker, A. J. 2000. Life history characteristics and the conservation of migratory shorebirds Gosling, L. M. Sutherland, W. J. Behaviour and Conservation. Cambridge University Press, Cambridge, United Kingdom 105 124.
41. Piersma, T. Carter, D. B. 2001. Red knots fattening on horseshoe crab eggs: body composition changes and energetics Wader Study Group Bull. 95: 13.
42. 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 Neth. J. Sea Res. 31: 331 357.
43. Piersma, T., Gudmundsson, G. A. Lilliendahl, K. 1999. Rapid changes in the size of different functional organs and muscle groups during refueling in a long-distance migrating shorebird Physiol. Biochem. Zool. 72: 405 415.
44. Piersma, T., Rogers, D. I., Gonzalez, P. M., Zwarts, L., Niles, L. J., de Lima Serrano do Nascimento, I., Minton, C. D.T. Baker, A. J. 2005. Fuel storage rates before northward flights in red knots worldwide: facing the severest ecological constraint in tropical intertidal environments? Greenberg, R. Marra, P. P. Birds of two worlds: ecology and evolution of migration. Johns Hopkins University Press, Baltimore 262 273.
45. - In: Rundel, P. W., Ehleringer, J. R. Nagy, K. A. Stable isotopes in ecological research. Springer-Verlag, New York 1989 Botton, M. L. 1985. A contribution to the population biology of horseshoe crabs, Limulus polyphemus (L.), in Delaware Bay Estuaries 8: 363 372.
46. Sitters, H. P., Gonzalez, P. M., Piersma, T., Baker, A. J. Price, D. J. 2001. Day and night feeding habitat of red knots in Patagonia: profitability versus safety? J. Field. Ornithol. 72: 86 95.
47. 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: 21.
48. Skagen, S. K. 2006. Migration stopovers and the conservation of Arctic-breeding calidridine sandpipers Auk 123: 313 322.
49. Smith, D. R., Millard, M. J. Eyler, S. 2006. Abundance of adult horseshoe crabs (Limulus polyphemus) in Delaware Bay estimated from a bay-wide mark-recapture study Fish. Bull. 104: 456 464.
50. Sperry, C. C. 1940. Food habits of a group of shorebirds: woodcock, snipe, knot, and dowitcher U.S. Dept. Int., Bur. Biol. Surv., Wildl. Res. Bull. 1. Washington, D.C.
51. Tieszen, L. L., Boutton, T. W., Tesdahl, K. G. Slade, N. A. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13 C analysis of diet Oecologia 57: 32 37.
52. Tsipoura, N. Burger, J. 1999. Shorebird diet during spring migration stopover on Delaware Bay Condor 101: 635 644.
53. van Gils, J. A., Piersma, T., Dekinga, A. Dietz, M. W. 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 3380.
54. Walls, E. A., Berkson, J. Smith, S. A. 2002. The horseshoe crab, Limulus polyphemus: 200 million years of existence, 100 years of study Rev. Fish. Sci. 10: 39 73.