Position of horseshoe crabs in estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition

Journal of Experimental Marine Biology and Ecology

Volumn 299, Issue 2, 2004, Pages 231-253

  Carmichael, Ruth H ^a   Rutecki, Deborah ^a   Annett, Brendan ^a   Gaines, Emily ^b   Valiela, Ivan ^a  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Bivalve; Crustacean; Gastropod; Limulus polyphemus; Organic matter; Polychaete

Indexed keywords

CRAB; DIET; ESTUARINE ECOSYSTEM; FOOD WEB; FORAGING BEHAVIOR; ORGANIC MATTER; PREDATOR;

CAPE COD; MASSACHUSETTS; NORTH AMERICA; PLEASANT BAY; UNITED STATES;

ALGAE; BIVALVIA; CRUSTACEA; DECAPODA (CRUSTACEA); GADUS MORHUA; GASTROPODA; LIMULUS; LIMULUS POLYPHEMUS; MEROSTOMATA; POLYCHAETA; POLYPHEMUS; SPARTINA;

EID: 1042275492     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2003.09.006     Document Type: Article

References (80)

1. Alexander S.A., Hobson K.A., Gratto-Trevor C.L., Diamond A.W. Conventional and isotopic determinations of shorebird diets at an inland stopover: the importance of invertebrates and Potamogeton pectinatus tubers. Can. J. Zool. 74:1996;1057-1068.
2. Alisauskas R.T., Hobson K.A. Determination of lesser snow goose diets and winter distribution using stable isotope analysis. J. Wildl. Manage. 57:1993;49-54.
3. Altabet M.A., Small L.F. Nitrogen isotopic ratios in fecal pellets produced by marine zooplankton. Geochim. Cosmochim. Acta. 54:1990;155-163.
4. Baptist J.P., Smith O.R., Ropes J.W. Migrations of the horseshoe crab, Limulus polyphemus, in Plum Island Sound, Massachusetts. U.S. Fish and Wildlife Service Special Scientific Report - Fisheries. vol. 220:1957;1-15.
5. Benner R., Kaiser K. Abundance of amino sugars and peptidoglycan in marine particulate and dissolved organic matter. Limnol. Oceanogr. 48:2003;118-128.
6. Berkson J., Shuster C. The horseshoe crab: the battle for a true multiple-use resource. Fish Manag. 24:1999;6-10.
7. Best P.B., Schell D.M. Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Mar. Biol. 124:1996;483-494.
8. Botton M.L. Predation of commercially important bivalve species in New Jersey by the horseshoe crab Limulus polyphemus (Linnaeus). J. Shellfish Res. 2:1982;89-90.
9. Botton M.L. Diet and food preferences of the adult horseshoe crab Limulus polyphemus in Delaware Bay, New Jersey, USA. Mar. Biol. 81:1984;199-207.
10. Botton M.L. The importance of predation by horseshoe crabs, Limulus polyphemus, to an intertidal sand flat community. J. Mar. Res. 42:1984;139-161.
11. Botton M.L. The conservation of horseshoe crabs: what can we learn from the Japanese experience? Tanacredi J. Limulus in the Limelight: A species 350 Million Years in the Making and in Peril? 2001;47-51 Kluwer Academic Publishing, NY.
12. Botton M.L., Haskin H.H. Distribution and feeding of the horseshoe crab, Limulus polyphemus, on the continental shelf off New Jersey. Fish Bull. 82:1984;383-389.
13. Botton M.L., Ropes J.W. Feeding ecology of horseshoe crabs on the continental shelf, New Jersey to North Carolina. Bull. Mar. Sci. 45:1989;637-647.
14. Breitburg D. Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheries. Estuaries. 25:2002;767-781.
15. Cabana G., Rasmussen J.B. Modeling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature. 372:1994;255-257.
16. Carmichael R.H., Rutecki D., Valiela I. Abundance and population structure of the Atlantic horseshoe crab, Limulus polyphemus, in Pleasant Bay, Cape Cod. Mar. Ecol. Prog. Ser. 246:2003;239-255.
17. Carmichael, R.H., Annett, B., Valiela, I., in press. Nitrogen loading to Pleasant Bay, Cape Cod: application of models and stable isotopes to detect incipient nutrient enrichment of estuaries. Mar. Poll. Bull.
18. Checkley D.M., Entzeroth L.C. Elemental and isotopic fractionation of carbon and nitrogen by marine, planktonic copepods and implications to the marine nitrogen cycle. J. Plankton Res. 7:1985;553-568.
19. Commito J.A., Currier C.A., Kane L.R., Reinsel K.A., Ulm I.M. Dispersal dynamics of the bivalve Gemma gemma in a patchy environment. Ecol. Monogr. 65:1995;1-20.
20. Creach V., Schricke M.T., Bertru G., Mariotti A. Stable isotopes and gut analyses to determine feeding relationships in saltmarsh macroconsumers. Estuar. Coast. Shelf Sci. 44:1997;599-611.
21. DeNiro M.J., Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta. 42:1978;495-506.
22. Evgenidou A., Valiela I. Response of growth and density of a population of Geukensia demissa to land-derived nitrogen loading, in Waquoit Bay, Massachusetts. Estuar. Coast. Shelf Sci. 55:2002;125-138.
23. 15N relationships. Mar. Ecol. Prog. Ser. 174:1998;301-306.
24. Franco-Nava M.A., Blancheton J.P., Deviller G., LeGall J.Y. Using stable isotopes to trace particulate organic matter transformations in a recirculating aquaculture system. Sea Farming Today and Tomorrow, Abstracts and short communications. EAS Special Publication. vol. 32:2002;242-243 Aquacult. Europe, Trieste, Italy.
25. Gaines E.F., Carmichael R., Grady S., Valiela I. Stable isotopic evidence for changing nutritional sources of juvenile horseshoe crabs. Biol. Bull. 203:2002;228-230.
26. Goldman J. Identification of nitrogen as a growth limiting nutrient in wastewaters and coastal marine waters through continuous culture algal assays. Water Res. 10:1975;97-104.
27. Gordon D.C. The effects of the deposit feeding polychaete Pectinaria gouldii on the intertidal sediments of Barnstable Harbor. Limnol. Oceanogr. 11:1966;327-332.
28. Gorokhova E., Hansson S. An experimental study on variation in stable carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Can. J. Fish. Aquat. Sci. 56:1999;2203-2210.
29. Griffin M.P.A., Valiela I. Delta super(15)N isotope studies of life history and trophic position of Fundulus heteroclitus and Menidia menidia. Mar. Ecol. Prog. Ser. 214:2001;299-305.
30. Harvey C.J., Hanson P.C., Essington T.E., Brown P.B., Kitchell J. Using bioenergetics models to predict stable isotope ratios in fishes. Can. J. Fish Aquat. Sci. 59:2002;115-124.
31. Hansson S., Hobbie J.E., Elmgren R., Larsson U., Fry B., Johansson S. The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology. 78:1997;2249-2257.
32. Hesslein R.H., Capel M.J., Fox D.E., Hallard K.A. Stable isotopes of sulfur, carbon, and nitrogen, as indicators of trophic level and fish migration in the lower Mackenzie River Basin, Canada. Can. J. Fish. Aquat. Sci. 48:1991;2258-2265.
33. Hyslop E.J. Stomach contents analysis - a review of methods and their application. J. Fish Biol. 17:1980;411-429.
34. Kamermans P. Similarity in food source and timing of feeding in deposit- and suspension-feeding bivalves. Mar. Ecol. Prog. Ser. 104:1994;63-75.
35. Kang C.K., Sauriau P.G., Richard P., Blanchard G.F. Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oleron Bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar. Ecol. Prog. Ser. 187:1999;147-158.
36. 13C value of faecal pellets. Mar. Ecol. Prog. Ser. 240:2002;195-204.
37. Kline T.C. Jr., Wilson W.J., Goering J.J. Natural isotope indicators of fish migration at Prudhoe Bay, Alaska. Can. J. Fish Aquat. Sci. 55:1998;1494-1502.
38. Kraeuter J.N., Fegley S.R. Vertical disturbance of sediments by horseshoe crabs (Limulus polyphemus) during their spawning season. Estuaries. 17:1994;288-294.
39. Lafon M. Sur la composition du tégument des crustacés. C. R. Seances. Soc. Biol. Paris. 135:1941;1003-1007.
40. Lawton P., Lavalli K.L. Postlarval, juvenile, adolescent, and adult ecology. Factor J.R. Biology of the Lobster Homarus americanus. 1995;47-88 Academic Press, San Diego.
41. Mayer B., Boyer E.W., Goodale C., Jaworski N.A., Van Breemen N., Howarth R.W., Seitzinger S., Billen G., Lajtha K., Nadelhoffer K., Van Dam D., Hetling L.J., Nosal M., Paustian K. Sources of nitrate in rivers draining sixteen watersheds in the northeastern U.S.: isotopic constraints. Biogeochemistry. 57/58:2002;171-197.
42. McClelland J.W., Valiela I. Linking nitrogen in estuarine producers to land-derived sources. Limnol. Oceanogr. 43:1998;577-585.
43. McClelland J.W., Valiela I. Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Mar. Ecol. Prog. Ser. 168:1998;259-271.
44. McClelland J.W., Valiela I., Michener R.H. Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnol. Oceanogr. 42:1997;930-937.
45. McDermott J.J. The distribution and food habits of Nephtys bucera Ehlers, 1868 (Polychaeta: Nephtyidae) in the surf zone of a sandy beach. Proc. Biol. Soc. Wash. 100:1987;21-27.
46. McGinnis T.W., Emslie S.D. The foraging ecology of royal and sandwich terns in North Carolina, USA. Waterbirds. 3:2001;361-370.
47. Michels S.F. Summary of trends in horseshoe crab abundance in Delaware. Farrell J., Martin C. Proceedings of the Horseshoe Crab Forum: Status of the Resource. 1996;26-29 University of Delaware Sea Grant College Program, Lewes, DE.
48. Michener R.H., Schell M. Stable isotope ratios as tracers in marine aquatic food webs. Lajtha K., Michener R.H. Stable Isotopes in Ecology and Environmental Science. 1994;138-158 Blackwell Scientific.
49. 15N in particulate nitrogen and zooplankton in the Gulf Stream region and warm-core ring 86A. Deep-Sea Res. 39:1992;S363-S392. (Suppl.).
50. Peterson B.J., Fry B. Stable isotopes in ecosystem studies. Ann. Rev. Ecolog. Syst. 18:1987;293-320.
51. Prins T.C., Escaravage V., Wetsteyn L.P.M.J., Peeters J., Smaal A.C. Effects of different N- and P-loading on primary and secondary production in an experimental marine ecosystem. Aquat. Ecol. 33:1999;65-81.
52. Redmond M.S., Scott K.J. Amphipod predation by infaunal polychaete, Nephtys incisa. Estuaries. 12:1989;205-207.
53. Riska B. Morphological variation in the horseshoe crab Limulus polyphemus. Evolution. 35:1981;647-658.
54. RMP, 1998. Pleasant Bay Resource Management Plan. Pleasant Bay Technical Advisory Committee and Ridley and Associates. 179 pp.
55. Rudloe A. Locomotor and light responses of larvae of the horseshoe crab, Limulus polyphemus (L.). Biol. Bull. 157:1979;494-505.
56. Rudloe A. Aspects of the biology of juvenile horseshoe crabs, Limulus polyphemus. Bull. Mar. Sci. 31:1981;125-133.
57. Rudloe A. Man's influence as an environmental threat to Limulus. Bonaventuraet al. Physiology and Biology of Horseshoe Crabs: Studies on Normal and Environmentally Stressed Animals. Progress in Clinical and Biological Research. vol. 81:1982;297-300 Alan R. Liss, New York, NY.
58. Rudloe A. Variation in the expression of lunar and tidal behavioral rhythms in the horseshoe crab, Limulus polyphemus. Bull. Mar. Sci. 36:1985;388-395.
59. Ruppert E., Barnes R. Invertebrate Zoology. 1994;Sanders College Publishing. 1056 pp.
60. Schmidt K., Atkinson A., Stübing D., McClelland M., Montoya J., Voss M. Trophic relationships among Southern Ocean copepods and krill: some uses and limitation of a stable isotope approach. Limnol. Oceanogr. 48:2003;277-289.
61. Sekiguchi K. Biology of Horseshoe Crabs. 1988;Science House, Tokyo. 428 pp.
62. Shriver A.C., Carmichael R.H., Valiela I. Growth, condition, reproductive potential, and mortality of bay scallops, Argopecten irradians, in response to eutrophic-driven changes in food resources. J. Exp. Mar. Biol. Ecol. 279:2002;21-40.
63. Shuster, C.N., Jr., 1955. On morphometric and serological relationships within the Limulidae, with particular reference to Limulus polyphemus (L.). PhD thesis, New York University.
64. Shuster C.N. Jr. A pictorial review of the natural history and ecology of the horseshoe crab Limulus polyphemus, with reference to other Limulidae. Bonaventura J.et al. Physiology and Biology of Horseshoe Crabs. Studies on Normal and Environmentally Stressed Animals. Progress in Clinical and Biological Research. vol. 81:1982;1-52 Alan R. Liss, New York, NY.
65. Shuster C.N. Jr. Abundance of adult horseshoe crabs, Limulus polyphemus, in Delaware Bay, 1850-1990. Farrell J., Martin C. Proceedings of the Horseshoe Crab Forum: Status of the Resource. 1996;5-14 University of Delaware Sea Grant College Program, Lewes, DE.
66. Smith V.H., Tilman G.D., Nekola J.C. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ. Pollut. 100:1999;179-196.
67. Sokal R.R., Rohlf F.J. Biometry. 1981;500-530 W. H. Freeman, San Francisco.
68. 15N for tracer studies. J. Agric. Sci., Cambridge. 90:1978;7-9.
69. Sutela T., Huusko A. Varying resistance of zooplankton prey to digestion: implications for quantifying larval fish diets. Trans. Am. Fish. Soc. 129:2000;545-551.
70. Swan B.L., Hall W.R., Shuster C. Annual survey of horseshoe crab spawning activity along the shores of Delaware Bay, 1990-1995 summary. Farrell J., Martin C. Proceedings of the Horseshoe Crab Forum: Status of the Resource. 1996;35-49 University of Delaware Sea Grant College Program, Lewes, DE.
71. Tanacredi J.T. Horseshoe crabs imperiled? The fate of a species 350 million years in the making. Tanacredi J. Limulus in the Limelight: A species 350 Million Years in the Making and in Peril? 2001;7-14 Kluwer Academic Publishing, NY.
72. Valiela I. Marine Ecological Processes. 1995;203-212 Springer, NY.
73. Valiela I., Foreman K., LaMontagne M., Hersh D., Costa J., Peckol P., DeMeo-Anderson B., D'Avanzo C., Babione M., Sham C., Brawley J., Lajtha K. Couplings of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries. 15:1992;443-457.
74. Valiela I., Collins G., Kremer J., Lajtha K., Geist M., Seely B., Brawley J., Sham C.H. Nitrogen loading from coastal waters to receiving estuaries: new method and application. Ecol. Appl. 7:1997;358-380.
75. 13C trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 46:2001;2061-2066.
76. Voss M., Struck U. Stable nitrogen and carbon isotopes as indicator of eutrophication of the Oder River (Baltic Sea). Mar. Chem. 59:1997;35-49.
77. Waldron S., Tatner P., Jack I., Arnott C. The impact of sewage discharge in a marine embayment: a stable isotope reconnaissance. Estuar. Coast. Shelf Sci. 52:2001;111-115.
78. Walker J.L., Potter C.W., Macko S.A. The diets of modern and historic bottlenose dolphin populations reflected through stable isotopes. Mar. Mamm. Sci. 15:1999;335-350.
79. Weiss E.T., Carmichael R.H., Valiela I. The effect of nitrogen loading on the growth rates of quahogs (Mercenaria mercenaria) and soft-shell clams (Mya arenaria) through changes in food supply. Aquaculture. 211:2002;275-289.
80. Widener J.W., Barlow R.B. Decline of a horseshoe crab population on Cape Cod. Biol. Bull. 197:1999;300-302.