Effects of shorebird predation and snail abundance on an intertidal mudflat community

Journal of Sea Research

Volumn 92, Issue , 2014, Pages 102-114

  Cheverie, Anne V ^a   Hamilton, Diana J ^a   Coffin, Michael R S ^a,b,c   Barbeau, Myriam A ^b  

^a MOUNT ALLISON UNIVERSITY   (Canada)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

^c UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

Author keywords

Calidris pusilla; Community dynamics; Corophium volutator; Intertidal mudflat; Nassarius obsoletus; Trophic cascade

Indexed keywords

ABUNDANCE; AMPHIPOD; CHLOROPHYLL A; COMMUNITY STRUCTURE; DIATOM; INTRAGUILD PREDATION; MUDFLAT; OMNIVORY; PREDATION; SNAIL; TROPHIC CASCADE; WADER;

ATLANTIC OCEAN; BAY OF FUNDY; CANADA;

EID: 84907140896     PISSN: 13851101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.seares.2014.03.011     Document Type: Article

References (103)

1. Anderson M.J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 2006, 62:245-253.
2. Anderson M.J., Gorley R.N., Clarke K.R. PERMANOVA+ for Primer: Guide to software and statistical methods 2008, PRIMER-E, Plymouth, UK.
3. Armitage A.R., Fong P. Predation and physical disturbance by crabs reduce the relative impacts of nutrients in a tidal mudflat. Mar. Ecol. Prog. Ser. 2006, 313:205-213.
4. Armitage A.R., Gonzalez V.L., Fong P. Decoupling of nutrient and grazer impacts on a benthic estuarine diatom assemblage. Estuar. Coast. Shelf Sci. 2009, 84:375-382.
5. Armonies W. Active emergence of meiofauna from intertidal sediment. Mar. Ecol. Prog. Ser. 1988, 43:151-159.
6. Aubut A.V. Trophic Interactions on an Intertidal Mudflat: The Effects of Nutrient Availability, Mudsnail (Ilyanassa obsoleta) Abundance and Semipalmated Sandpiper (Calidris pusilla) Predation. B. Sc. Honours Thesis 2008, Mount Allison University, Sackville, New Brunswick, Canada.
7. Barbeau M.A., Grecian L.A., Arnold E.E., Sheahan D.C., Hamilton D.J. Spatial and temporal variation in the population dynamics of the intertidal amphipod C. volutator in the upper Bay of Fundy, Canada. J. Crustac. Biol. 2009, 29:491-506.
8. Bell S.S., Walters K., Hall M.O. Habitat utilization by harparcticoid copepods: a morphometric approach. Mar. Ecol. Prog. Ser. 1987, 35:59-64.
9. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Stat Methodol.) 1995, 57:289-300.
10. Best R.J., Stachowicz J.J. Trophic cascades in seagrass meadows depend on mesograzer variation in feeding rates, predation susceptibility, and abundance. Mar. Ecol. Prog. Ser. 2012, 456:29-42.
11. Boates J.S., Smith P.C. Crawling behaviour of the amphipod Corophium volutator and foraging by Semipalmated Sandpipers, Calidris pusilla. Can. J. Zool. 1989, 67:457-462.
12. Boates J.S., Forbes M., Zinck M., McNeil N. Male amphipods (Corophium volutator [Pallas]) show flexible behaviour in relation to risk of predation by sandpipers. Ecoscience 1995, 2:123-128.
13. Bringloe T.T., Drolet D., Barbeau M.A., Forbes M.R., Gerwing T.G. Spatial variation in population structure and its relation to movement and the potential for dispersal in a model intertidal invertebrate. PLoS One 2013, 8(7):e69091. 10.1371/journal.pone.0069091.
14. Buffan-Dubau E., Carman K.R. Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnol. Oceanogr. 2000, 45:381-395.
15. Clarke K.R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 1993, 18:117-143.
16. Clarke K.R., Gorley R.N. PRIMER v6: User Manual/Tutorial 2006, PRIMER-E, Plymouth, UK.
17. Coffin M.R.S., Drolet D., Hamilton D.J., Barbeau M.A. Effect of immersion at low tide on distribution and movement of the mud snail, Ilyanassa obsoleta (Say), in the upper Bay of Fundy, eastern Canada. J. Exp. Mar. Biol. Ecol. 2008, 364:110-115.
18. Coffin M.R.S., Barbeau M.A., Hamilton D.J., Drolet D. Effect of the mud snail Ilyanassa obsoleta on vital rates of the intertidal amphipod Corophium volutator. J. Exp. Mar. Biol. Ecol. 2012, 418-419:12-23.
19. Commito J.A. Importance of predation by infaunal polychaetes in controlling the structure of a soft-bottom community in Maine, USA. Mar. Biol. 1982, 68:77-81.
20. Connor M.S., Teal J.M., Valiela I. The effect of feeding by mudsnails, Ilyanassa obsoleta (Say), on the structure and metabolism of a laboratory benthic algal community. J. Exp. Mar. Biol. Ecol. 1982, 65:29-45.
21. Consalvey M., Paterson D.M., Underwood G.J.C. The ups and downs of life in a benthic biofilms: migration of benthic diatoms. Diatom Res. 2004, 19:181-202.
22. Coulthard M.E., Hamilton D.J. Effects of Ilyanassa obsoleta (Say) on the abundance and vertical distribution of Corophium volutator (Pallas) on mudflats of the upper Bay of Fundy. J. Exp. Mar. Biol. Ecol. 2011, 397:161-172.
23. Cranford P.J. Behaviour and ecological importance of a mud snail (Ilyanassa obsoleta) population in a temperate macrotidal estuary. Can. J. Zool. 1988, 66:459-466.
24. Crewe T.L., Hamilton D.J., Diamond A.W. Effects of mesh size on sieved samples of Corophium volutator. Estuar. Coast. Shelf Sci. 2001, 53:151-154.
25. Curtis L.A., Hurd L.E. On the broad nutritional requirements of the mud snail, Ilyanassa (Nassarius) obsoleta (Say), and its polytrophic role in the food web. J. Exp. Mar. Biol. Ecol. 1979, 41:289-297.
26. Curtis L.A., Hurd L.E. Nutrient procurement strategy of a deposit feeding estuarine neogastropod, Ilyanassa obsoleta. Estuar. Coast. Shelf Sci. 1981, 13:277-285.
27. Daborn G.R., Amos C.L., Brylinsky M., Christian H., Drapeau G., Faas R.W., Grant J., Long B., Paterson D.M., Perillo G.M.E., Piccolo M.C. An ecological cascade effect: migratory birds affect stability of intertidal sediments. Limnol. Oceanogr. 1993, 38:225-231.
28. Drolet D., Barbeau M.A., Coffin M.R.S., Hamilton D.J. Effect of the snail Ilyanassa obsoleta (Say) on dynamics of the amphipod Corophium volutator (Pallas) on an intertidal mudflat. J. Exp. Mar. Biol. Ecol. 2009, 368:189-195.
29. Drolet D., Coffin M.R.S., Barbeau M.A., Hamilton D.J. Influence of intra- and interspecific interactions on short-term movement of the amphipod Corophium volutator in varying environmental conditions. Estuar. Coasts 2013, 10.1007/s12237-013-9605-4.
30. Drolet D., Kennedy K., Barbeau M.A. Winter population dynamics and survival strategies of the intertidal mudflat amphipod Corophium volutator (Pallas). J. Exp. Mar. Biol. Ecol. 2013, 441:126-137.
31. Estes J.A., Palmisano J.A. Sea otters: their role in structuring nearshore communities. Science 1974, 185:1058-1060.
32. Estes J.A., Terborgh J., Brashares J.S., Power M.E., Berger J., Bond W.J., Carpenter S.R., Essington T.E., Holt R.D., Jackson J.B.C., Marquis R.J., Oksanen L., Oksanen T., Paine R.T., Pikitch E.K., Ripple W.J., Sandin S.A., Scheffer M., Schoener T.W., Shurin J.B., Sinclair A.R.E., Soulé M.E., Virtanen R., Wardle D.A. Trophic downgrading of planet earth. Science 2011, 333:301-306.
33. Fauchald K., Jumars P.A. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Annu. Rev. 1979, 17:193-284.
34. Feller R.J. Dietary immunoassay of Ilyanassa obsoleta, the eastern mud snail. Biol. Bull. 1984, 166:96-102.
35. Finke D.L., Denno R.F. Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol. Lett. 2005, 8:1299-1306.
36. Flach E.C. Disturbance of benthic infauna by sediment-reworking activities of the lugworm Arenicola marina. Neth. J. Sea Res. 1992, 30:81-89.
37. Fraterrigo J.M., Rusak J.A. Disturbance-driven changes in the variability of ecological patterns and processes. Ecol. Lett. 2008, 11:756-770.
38. Geider R.J. Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol. 1987, 106:1-34.
39. Gerdol V., Hughes R.G. Feeding behaviour and diet of Corophium volutator in an estuary in southeastern England. Mar. Ecol. Prog. Ser. 1994, 114:103-108.
40. Gerdol V., Hughes R.G. Effect of Corophium volutator on the abundance of benthic diatoms, bacteria and sediment stability in two estuaries in southeastern England. Mar. Ecol. Prog. Ser. 1994, 114:109-115.
41. Gilmurray M.C., Daborn G.R. Feeding relations of the Atlantic silverside Menidia menidia in the Minas Basin, Bay of Fundy. Mar. Ecol. Prog. Ser. 1981, 6:231-235.
42. Grant J., Bathmann U.V., Mills E.L. The interaction between benthic diatom films and sediment transport. Estuar. Coast. Shelf Sci. 1986, 23:225-238.
43. Gratto-Trevor C., Smith P.A., Morrison R.I.G., Aubry Y., Cotter R. Population trends in Semipalmated Sandpipers from migration counts. Waterbirds 2012, 35:96-105.
44. Guarini J.-M., Blanchard G.F., Gros Ph., Gouleau D., Bacher C. Dynamic model of the short-term variability of microphytobenthic biomass on temperate intertidal mudflats. Mar. Ecol. Prog. Ser. 2000, 195:291-303.
45. Hagerthey S.E., Defew E.C., Paterson D.M. Influence of Corophium volutator and Hydrobia ulvae on intertidal benthic diatom assemblages under different nutrient and temperature regimes. Mar. Ecol. Prog. Ser. 2002, 245:47-59.
46. Hairston N.G., Smith F.E., Slobodkin L.B. Community structure, population control, and competition. Am. Nat. 1960, 94:421-425.
47. Hamilton D.J. Direct and indirect effects of predation by common eiders and abiotic disturbance in an intertidal community. Ecol. Monogr. 2000, 70:21-43.
48. Hamilton D.J., Barbeau M.A., Diamond A.W. Shorebirds, mud snails, and Corophium volutator in the upper Bay of Fundy, Canada: predicting bird activity on intertidal mud flats. Can. J. Zool. 2003, 81:1358-1366.
49. Hamilton D.J., Diamond A.W., Wells P.G. Shorebirds, snails, and the amphipod (Corophium volutator) in the upper Bay of Fundy: top-down vs. bottom-up factors, and the influence of compensatory interactions on mudflat ecology. Hydrobiologia 2006, 567:285-306.
50. Hargrave B.T., Prouse N.J., Phillips G.A., Neame P.A. Primary production and respiration in pelagic and benthic communities at two intertidal sites in the upper Bay of Fundy. Can. J. Fish. Aquat. Sci. 1983, 40:229-243.
51. Hicklin P.W., Smith P.C. The diets of five species of migrant shorebirds in the Bay of Fundy. Proceedings of the Nova Scotian Institute of Science 1979, 29:483-488.
52. Hicklin P.W., Smith P.C. Selection of foraging sites and invertebrate prey by migrant Semipalmated Sandpipers, Calidris pusilla (Pallas), in Minas Basin, Bay of Fundy. Can. J. Zool. 1984, 62:2201-2210.
53. Hicklin P.W., Linkletter L.E., Peer D.L. Distribution and abundance of Corophium volutator (Pallas), Macoma balthica (L.) and Heteromastus filiformis (Clarapede) in the intertidal zone of Cumberland Basin and Shepody Bay, Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences No. 965 1980.
54. Hicks G.R.F., Coull B.C. The ecology of marine meiobenthic harpacticoid copepods. Oceanogr. Mar. Biol. Annu. Rev. 1983, 21:67-175.
55. Hooper D.U., Chapin F.S., Ewel J.J., Hector A., Inchausti P., Lavorel S., Lawton J.H., Lodge D.M., Loreau M., Naeem S., Schmid B., Setala H., Symstad A.J., Vandermeer J., Wardle D.A. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 2005, 75:3-35.
56. Jensen K.T., André C. Field and laboratory experiments on interaction among an infaunal polychaete, Nereis diversicolor, and two amphipods, Corophium volutator and C. arenarium: effects on survival, recruitment and migration. J. Exp. Mar. Biol. Ecol. 1993, 168:259-278.
57. Jokiel P.L., Morrisey J.I. Water motion on coral reefs: evaluation of the 'clod card' technique. Mar. Ecol. Prog. Ser. 1993, 93:175-181.
58. Kelaher B.P., Levinton J.S., Hoch J.M. Foraging by the mud snail, Ilyanassa obsoleta (Say), modulates spatial variation in benthic community structure. J. Exp. Mar. Biol. Ecol. 2003, 292:139-157.
59. Kuwae T., Miyoshi E., Hosokawa S., Ichimi K., Hosoya J., Amano T., Moriya T., Kondoh M., Ydenberg R.C., Elner R.W. Variable and complex food web structures revealed by exploring missing trophic links between birds and biofilm. Ecol. Lett. 2012, 15:347-356.
60. MacIntyre H.L., Geider R.J., Miller D.C. Microphytobenthos: the ecological role of the "secret garden" of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 1996, 19:186-201.
61. Matthews S.L., Boates J.S., Walde S.J. Shorebird predation may cause discrete generations in an amphipod prey. Ecography 1992, 15:393-400.
62. Mawhinney K., Hicklin P.W., Boates J.S. A re-evaluation of the numbers of migrant Semipalmated Sandpipers, Calidris pusilla, in the Bay of Fundy during fall migration. Can. Field-Nat. 1993, 107:19-23.
63. McCurdy D.G., Forbes M.R., Logan S.P., Lancaster D., Mautner S.I. Foraging and impacts by benthic fish on the intertidal amphipod Corophium volutator. J. Crustac. Biol. 2005, 25:558-564.
64. Mouritsen K.N., Mouritsen L.T., Jensen K.T. Change of topography and sediment characteristics on an intertidal mud-flat following mass-mortality of the amphipod Corophium volutator. J. Mar. Biol. Assoc. UK 1998, 78:1167-1180.
65. Minitab Inc Minitab Statistical Software, Release 16 for Windows 2010, State College, Pennsylvania, USA.
66. Nichols J.A., Robertson J.R. Field evidence that the eastern mud snail, Ilyanassa obsoleta, influences nematode community structure. Nautilus 1979, 93:44-46.
67. O'Gorman E.J., Emmerson M.C. Perturbations to trophic interactions and the stability of complex food webs. Proc. Natl. Acad. Sci. 2009, 106:13393-13398.
68. Ólafsson E.B., Persson L.-E. The interaction between Nereis diversicolor O.F. Müller and Corophium volutator Pallas as a structuring force in a shallow brackish sediment. J. Exp. Mar. Biol. Ecol. 1986, 103:103-117.
69. Pace M.L., Cole J.J., Carpenter S.R. Trophic cascades and compensation: differential response of microzooplankton in whole-lake experiments. Ecology 1998, 79:138-152.
70. Pace M.L., Cole J.J., Carpenter S.R., Kitchell J.F. Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 1999, 14:483-488.
71. Pascal P.-Y., Fleeger J.W., Boschker H.T.S., Mitwally H.M., Johnson D.S. Response of the benthic food web to short and long-term nutrient enrichment in saltmarsh mudflats. Mar. Ecol. Prog. Ser. 2013, 474:27-41.
72. Peer D.L., Linkletter L.E., Hicklin P.W. Life history and reproductive biology of Corophium volutator (Crustacea: Amphipoda) and the influence of shorebird predation on population structure in Chignecto Bay, Bay of Fundy, Canada. Neth. J. Sea Res. 1986, 20:359-373.
73. Perkins R.G., Underwood G.J.C., Brotas V., Snow G.C., Jesus B., Ribeiro L. Responses of microphytobenthos to light: primary production and carbohydrate allocation over an emersion period. Mar. Ecol. Prog. Ser. 2001, 223:101-112.
74. Pettibone M.H. Annelida. Synopsis and Classification of Living Organisms (v. 2) 1982, McGraw-Hill, New York, NY, USA. S.P. Parker (Ed.).
75. Pillay D., Branch G.M., Forbes A.T. Effects of Callianassa kraussi on microbial biofilms and recruitment of macrofauna: a novel hypothesis for adult-juvenile interactions. Mar. Ecol. Prog. Ser. 2007, 347:1-14.
76. Polis G.A., Strong D.R. Food web complexity and community dynamics. Am. Nat. 1996, 147:813-846.
77. Quammen M.L. Predation by shorebirds, fish, and crabs on invertebrates in intertidal mudflats: an experimental test. Ecology 1984, 65:529-537.
78. Quijón P.A., Snelgrove P.V.R. Trophic complexity in marine sediments: new evidence from the Gulf of St. Lawrence. Mar. Ecol. Prog. Ser. 2008, 371:85-89.
79. Quinn J.T., Hamilton D.J. Variation in diet of Semipalmated Sandpipers (Calidris pusilla) during stopover in the upper Bay of Fundy, Canada. Can. J. Zool. 2012, 90:1181-1190.
80. Raffaelli D., Milne H. An experimental investigation of the effects of shorebird and flatfish predation on estuarine invertebrates. Estuar. Coast. Shelf Sci. 1987, 24:1-13.
81. Rieper M. Feeding preferences of marine harpacticoid copepods for various species of bacteria. Mar. Ecol. Prog. Ser. 1982, 7:303-307.
82. Riera P., Richard P., Grémare A., Blanchard G. Food source of intertidal nematodes in the Bay of Marennes-Oléron (France), as determined by dual stable isotope analysis. Mar. Ecol. Prog. Ser. 1996, 142:303-309.
83. Robar N.D.P., Hamilton D.J. A method for estimating habitat use by shorebirds using footprints. Waterbirds 2007, 30:116-120.
84. Shepherd P.C., Boates J.S. Effects of a commercial baitworm harvest on Semipalmated Sandpipers and their prey in the Bay of Fundy Hemispheric Shorebird Reserve. Conserv. Biol. 1999, 13:347-356.
85. Silliman B.R., Bertness M.D. A trophic cascade regulates salt marsh primary production. Proc. Natl. Acad. Sci. 2002, 99:10500-10505.
86. Soluk D.A. Multiple predator effects: predicting combined functional response of stream fish and invertebrate predators. Ecology 1993, 74:219-225.
87. Strong D.R. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 1992, 73:747-754.
88. Stuart V., Head E.J.B., Mann K.H. Seasonal changes in the digestive enzyme levels of the amphipod Corophium volutator (Pallas) in relation to diet. J. Exp. Mar. Biol. Ecol. 1985, 88:243-256.
89. Sundback K., Nilsson P., Nilsson C., Jonsson B. Balance between autotrophic and heterotrophic components and processes in microbenthic communities of sandy sediments: a field study. Estuar. Coast. Shelf Sci. 1996, 43:689-706.
90. Thrush S.F. Complex role of predators in structuring soft-sediment macrobenthic communities: implications of changes in spatial scale for experimental studies. Aust. J. Ecol. 1999, 24:344-354.
91. Tietjen J.H. The ecology of shallow water meiofauna in two New England estuaries. Oecologia 1969, 2:251-291.
92. Trites M., Kaczmarska I., Ehrman J.M., Hicklin P.W., Ollerhead J. Diatoms from two macro-tidal mudflats in Chignecto Bay, upper Bay of Fundy, New Brunswick, Canada. Hydrobiologia 2005, 544:299-319.
93. Underwood A.J. Experiments in Ecology: their Logical Design and Interpretation using Analysis of Variance 1997, Cambridge University Press, Cambridge, UK.
94. Underwood G.J.C., Paterson D.M. Seasonal changes in diatom biomass, sediment stability and biogenic stabilization in the Severn estuary. J. Mar. Biol. Assoc. UK 1993, 73:871-887.
95. Warwick R.M. The level of taxonomic discrimination required to detect pollution effects on marine benthic communities. Mar. Pollut. Bull. 1988, 19:259-268.
96. Warwick R.M., Clarke K.R. Increased variability as a symptom of stress in marine communities. J. Exp. Mar. Biol. Ecol. 1993, 172:215-226.
97. Warwick R.M., Price R. Ecological and metabolic studies on free-living nematodes from an estuarine mud-flat. Estuar. Coast. Mar. Sci. 1979, 9:257-271.
98. Wilson W.H. Shifting zones in a Bay of Fundy soft-sediment community: patterns and processes. Ophelia 1988, 29:227-245.
99. Wilson W.H. Predation and the mediation of intraspecific competition in an infaunal community in the Bay of Fundy. J. Exp. Mar. Biol. Ecol. 1989, 132:221-245.
100. Wilson W.H. Relationship between prey abundance and foraging site selection by Semipalmated Sandpipers on a Bay of Fundy mudflat. J. Field Ornithol. 1990, 61:9-19.
101. Wilson W.H. The importance of epibenthic predation and ice disturbance in a Bay of Fundy mudflat. Ophelia Suppl. 1991, 5:507-514.
102. Woodin S.A. Polychaete abundance patterns in a marine soft-sediment environment: the importance of biological interactions. Ecol. Monogr. 1974, 44:171-187.
103. Woodin S.A., Wethey D.S., Volkenborn N. Infaunal hydraulic ecosystem engineers: cast of characters and impacts. Integr. Comp. Biol. 2010, 50:176-187.