Effects of seabird nesting colonies on algae and aquatic invertebrates in coastal waters

Marine Ecology Progress Series

Volumn 417, Issue , 2010, Pages 287-300

  Kolb, Gundula S ^a   Ekholm, Janna ^a   Hambäck, Peter A ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Baltic Sea; Bottom up; Cormorants; Eutrophication; Nitrogen; Stable isotopes

Indexed keywords

ARCHIPELAGO; BOTTOM-UP CONTROL; COASTAL ZONE; COLONY; CRUSTACEAN; EPIPHYTE; EUTROPHICATION; MARINE ECOSYSTEM; NEST; NESTING; NITROGEN; PHOSPHORUS; SEABIRD; SEAWEED; STABLE ISOTOPE; TOP-DOWN CONTROL;

ATLANTIC OCEAN; BALTIC SEA; STOCKHOLM [SWEDEN]; STOCKHOLM ARCHIPELAGO; SWEDEN;

ALGAE; CHIRONOMIDAE; FUCUS; FUCUS VESICULOSUS; GAMMARUS; INVERTEBRATA; JAERA ALBIFRONS; PHALACROCORACIDAE;

EID: 78149451812     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps08791     Document Type: Article

References (91)

1. Barnes RSK (1994) The brackish-water fauna of northwestern Europe. Cambridge University Press, New York
2. Barrett K, Anderson WB, Wait DA, Grismer LL, Polis GA, Rose MD (2005) Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos 109: 145-153
3. Berger R, Henriksson H, Kautsky L, Malm T (2003) Effects of filamentous algae and deposited matter on the survival of Fucus vesiculosus L. Germlings in the Baltic Sea. Aquat Ecol 37:1-11
4. Birt VL, Birt TP, Goulet D, Cairnse DK, Montevecchi WA (1987) Ashmole's halo: direct evidence for prey depletion by a seabird. Mar Ecol Prog Ser 40:205-208
5. Blumenshine SC, Vadeboncoeur Y, Lodge DM, Cottingham KL, Knight SE (1997) Benthic-pelagic links: responses of benthos to water-column nutrient enrichment. J N Am Benthol Soc 16:466-479
6. Bosman AL, Hockey PAR (1986) Seabird guano as a determinant of rocky intertidal community structure. Mar Ecol Prog Ser 32:247-257
7. Bosman AL, Hockey PAR (1988) The influence of seabird guano on the biological structure of rocky intertidal communities on islands off the west coast of southern Africa. SAfr J Mar Sci 7:61-68
8. Bosman AL, Dutoit JT, Hockey PAR, Branch GM (1986) A field experiment demonstrating the influence of seabird guano on intertidal primary production. Estuar Coast Shelf Sci 23:283-294
9. Bustamante RH, Branch GM (1996) Large scale patterns and trophic structure of southern African rocky shore: the role of geographic variation and wave exposure. J Biogeogr 23:339-351
10. 13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443-453
11. Clesceri LS, Greenberg AE, Eaton AD (1998). Standard methods for the examination of water and wastewater. American Public Health Association, New York
12. Dalton CM, Ellis D, Post DM (2009) The impact of double- crested cormorant (Phalacrocorax auritus) predation on anadromous alewife (Alosa pseudoharengus) in south- central Connecticut, USA. Can J Fish 66:177-180
13. De Jonge VM, Elliott M, Orive E (2002) Causes, historical development, effects and future challenges of a common environmental problem: eutrophication. Hydrobiologia 475(1):1-19
14. Draulans D (1988) Effects of fish-eating birds on fresh-water fish stocks- an evaluation. Biol Cons 44:251-263
15. Ellis JC (2005) Marine birds on land: a review of plant bio- mass, species richness, and community composition in seabird colonies. Plant Ecol 181:227-241
16. Ellis JC, Shulman MJ, Wood M, Witman JD, Lozyniak C (2007) Regulation of intertidal food webs by avian predators on New England rocky shores. Ecology 88:853-863
17. Elmgren R (2001) Understanding human impact on the Baltic ecosystem: changing views in recent decades. Ambio 30: 222-231
18. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR and others (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578-580
19. Elser JJ, Matthew MES, Cleland EE, Gruner DS and others (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135-1142
20. Engström H (2001) Long term effects of cormorant predation on fish communities and fishery in a freshwater lake. Ecography 24:127-138
21. Eriksson BK, Sandstrom A, Isaeus M, Schreiber H, Karås P (2004) Effects of boating activities on aquatic vegetation in the Stockholm archipelago, Baltic Sea. Estuar Coast Shelf Sci 61:339-349
22. Fry B (2006) Stable isotope ecology. Springer, New York
23. Goecker ME, Kall SE (2003) Grazing preferences of marine isopods and amphipods on three prominent algal species of the Baltic Sea. J Sea Res 50:309-314
24. Golovkin AN (1967) The effect of colonial sea birds on development of the phytoplankton. Oceanology (Mosc) 7: 521-529
25. Golovkin AN, Garkavaya GP (1975) Fertilization of waters off the Murmansk coast by bird excreta near various types of colonies. Sov J Mar Biol 1:345-351
26. Grover JP (1997) Resource competition. Chapman and Hall, London
27. Hahn S, Bauer S, Klaassen M (2007) Estimating the contribution of carnivorous waterbirds to nutrient loading in fresh- water habitats. Freshw Biol 52:2421-2433
28. Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food algae. Ecology 83:1052-1064
29. Hutchinson GE (1950) Survey of existing knowledge of biogeochemistry. 3. The biogeochemistry of vertebrate excretion. Bull Am Mus Nat Hist 96:1-554
30. Jormalainen V, Honkanen T, Heikkilä N (2001) Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220: 219-230
31. Karez R, Engelbert S, Sommer U (2000) 'Co-consumption' and 'protective coating': two new proposed effects of epiphytes on their macroalgal hosts in mesograzer-epiphyte- host interactions. Mar Ecol Prog Ser 205:85-93
32. Keatley BE, Douglas MSV, Blais JM, Mallory ML, Smol JP (2009) Impacts of seabird-derived nutrients on water quality and diatom assemblages from Cape Vera, Devon Island, Canadian High Artic. Hydrobiol 621:191-205
33. Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing delta C-13 values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43:1213-1222
34. Kolb GS, Jerling L, Hambäck PA (2010) The impact of cormorants on plant-arthropod food webs on their nesting islands. Ecosystems 13:353-366
35. Korpinen S, Jormalainen V, Honkanen T (2007) Effects of nutrients, herbivory, and depth on the marcoalgae community in the rocky sublittoral. Ecology 88:839-852
36. Korpinen S, Jormalainen V, Ikonen J (2008) Selective consumption and facilitation by mesograzers in adult and colonizing macroalgal assemblages. Mar Biol 154:787-794
37. Korpinen S, Jormalainen V, Pettay E (2010) Nutrient availability modifies abundance and community structure of Fucus-associated littoral benthic fauna. Mar Environ Res 70:283-292
38. Kotta J, Paalme T, Martin G, Makinen A (2000) Major changes in macroalgae community composition affect the food and habitat preference of Idotea baltica. Int Rev Hydrobiol 85:697-705
39. Kraufvelin P (2007) Responses to nutrient enrichment, wave action and disturbance in rocky shore communities. Aquat Bot 87:262-274
40. Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R, Pedersen MF (2006) Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199-209
41. Kurle CM, Croll DA, Tershy BR (2008) Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated. Proc Natl Acad Sci 105:3800-3804
42. Lapointe BE, Littler MM, Littler DS (1992) Nutrient availability to marine macroalgae in siliciclastic versus carbonate- rich coastal waters. Estuaries 15:75-82
43. Lehikoinen A (2005) Prey-switching and diet of the great cormorant during the breeding season in the Gulf of Finland. Waterbirds 28:511-515
44. Liess A, Haglund AL (2007) Periphyton responds differentially to nutrients recycled in dissolved or faecal pellet form by the snail grazer Theodoxus fluviatilis. Freshw Biol 52:1997-2008
45. Lindeboom HJ (1984) The nitrogen pathway in a penguin rookery. Ecology 65:269-277
46. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, New York
47. Loder TC III, Ganning B, Love JA (1996) Ammonia nitrogen dynamics in costal rockpools affected by gull guano. J Exp Mar Biol Ecol 196:113-129
48. Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77: 838-846
49. Malm T, Isaeus M (2005) Distribution of marcoalgal communities in the central Baltic Sea. Ann Bot Fenn 42:257-266
50. Marion L, Clergeau, Brient L, Bertru G (1994) The importance of avian-contributed nitrogen (N) and phosphorus (P) to Lake Grand Lieu, France. Hydrobiologia 279-280: 133-147
51. Mattson WJ (1980) Herbivory in relation to plant nitrogen- content. Annu Rev Ecol Syst 11:119-161
52. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378-390
53. Michelutti N, Keatley BE, Brimble S, Blais JM and others (2009) Seabird-driven shifts in Arctic pond ecosystems. Proc Biol Sci 276:591-596
54. Mizutani H, Hasegawa H, Wada E (1986) High nitrogen isotope ratio for soils of seabird rookeries. Biochem 2: 221-247
55. Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470-480
56. Onuf CP, Teal JM, Valiela I (1977) Interactions of nutrients, plants growth and herbivory in a mangrove ecosystem. Ecology 58:514-526
57. Orav-Kotta H, Kotta J (2004) Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiol 514:79-85
58. Osono T, Hobara S, Fujiwara, Koba K, Kameda K (2002) Abundance, diversity, and species composition of fungal communities in a temperate forest affected by excreta of the Great Cormorant Phalacrocorax carbo. Soil Biol Biochem 34:1537-1547
59. Paillisson JM, Carpentier A, Le Gentil J, Marion L (2004) Space utilization by a cormorant (Phalacrocorax carbo L.) colony in a multi-wetland complex in relation to feeding strategies. C R Biol 327:493-500
60. Palomo G, Iribarne O, Martinez MM (1999) The effect of migratory seabirds guano on the soft bottom community of a SW Atlantic coastal lagoon. Bull Mar Sci 65:119-128
61. Pavia H, Carr H, Åberg P (1999) Habitat and feeding preferences of crustacean mesoherbivores inhabiting the brown seaweed Asophyllum nodosum (L.) Le Jol. and its epiphytic marcoalgae. J Exp Mar Biol Ecol 236:15-32
62. Pedersen MF, Borum J (1996) Nutrient reference of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar Ecol Prog Ser 142:261-272
63. Polis GA, Hurd SD (1995) Extraordinarily high spider densities on islands - flow of energy from the marine to terrestrial food webs and the absence of predation. Proc Natl Acad Sci USA 92:4382-4386
64. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179-189
65. Postel SL, Carpenter SR (1997) Freshwater ecosystem services. In: Daily G (ed) Nature's services. Island Press, Washington, DC, p 195-214
66. Råberg S, Kautsky L (2007) A comparative biodiversity study of the associated fauna of perennial fucoids and filamentous algae. Estuar Coast Shelf Sci 73:249-258
67. Raberg S, Kautsky L (2008) Grazer identity is crucial for facilitating growth of the perennial brown alga Fucus. Mar Ecol Prog Ser 361:111-118
68. Rolff C, Elmgren R, Voss M (2008) Deposition of nitrogen and phosphorus on the Baltic Sea: seasonal patterns and nitrogen isotope composition. Biogeosciences 5:1657-1667
69. Rönnberg C, Bonsdorff E (2004) Baltic Sea eutrophication: area-specific ecological consequences. Hydrobiologia 514: 227-241
70. Schmidt S, Dennison WC, Moss GJ, Stewart GR (2004) Nitrogen ecophysiology of Heron Islands, a subtropical coral cay of the Great Barrier Reef, Australia. Funct Plant Biol 31:517-528
71. Schwoerbel J (ed) (1993) Einführung in die Limnologie, 7. Aufl. Gustav Fischer Verlag, Stuttgart/Jena/New York
72. Sjoberg B (1967) On the ecology of the Jaera albifrons group (Isopoda). Sarsia 29:321-348
73. Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems - a global problem. Environ Sci Poll Res 10:126-139
74. Staav R (2008) Skarv. In: Standfager K, Palmblad U (eds) Levande skärgårdsnatur 2008-med rapporter från 2007. Skärgårdsstiftelsen, Stockholm
75. Staav R (2009) Ringmärkning av kustfåglar. In: Wibjörn C, Palmblad U (eds) Levande skärgårdsnatur 2009-med rapporter från 2007. Skärgårdsstiftelsen, Stockholm
76. Staav R (2010) Ringmärkning av kustfåglar. In: Standfager K, Palmblad U (eds) Levande skärgårdsnatur 2010-med rapporter från 2007. Skärgårdsstiftelsen, Stockholm
77. Staunton Smith J, Johnson CR (1995) Nutrient inputs from seabirds and humans on a populated coral cay. Mar Ecol Prog Ser 124:189-200
78. Takamura N, Iwakuma T (1991) Nitrogen uptake and C-N-O ratio of epiphytic algae in the littoral zone of Lake Kasum- igaura. Arch Hydrob 121:161-170
79. Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, NJ
80. Towns DR, Wardle DA, Mulder CPH, Yeates GW and others (2009) Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118:420-430
81. Vander Zanden MJ, Rasmussen JB (1999) Primary consumer delta C-13 and delta N-15 and the trophic position of aquatic consumers. Ecology 80:1395-1404
82. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet delta N-15 enrichment: a meta-analysis. Oecologia 136:169-182
83. Voss M, Deutsch B, Elmgren R, Humborg C and others (2006) Source identification of nitrate by means of isotopic tracers in the Baltic Sea catchment. Biogeosciences 3:663-676
84. Wainright SC, Haney JC, Kerr C, Golovkin AN, Flint MV (1998) Utilization of nitrogen derived from seabird guano by terrestrial and marine plants at St. Paul, Pribilof Islands, Bering Sea, Alaska. Mar Biol 131:63-71
85. Wikstrom SA, Kautsky L (2007) Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuar Coast Shelf Sci 72:168-176
86. Wootton JT (1991) Direct and indirect effects of nutrients on intertidal community structure-variable consequences of seabird guano. J Exp Mar Biol Ecol 151:139-153
87. Wootton JT (1992). Indirect effects, prey susceptibility, and habitat selection-impacts of birds on limpets and algae. Ecology 73:981-991
88. Worm B, Sommer U (2000) Rapid direct and indirect effects of a single nutrient pulse in a seaweed-epiphyte-grazer system. Mar Ecol Prog Ser 202:283-288
89. Worm B, Lotze HK, Sommer U (2000) Coastal food web structure, carbon storage, and nitrogen retention regulated by consumer pressure and nutrient loading. Limnol Oceanogr 45:339-349
90. Young HS, Hurrey L, Kolb GS (2011) Effects of seabird- derived nutrients on aquatic systems. In: Mulder CPH, Anderson WB, Towns DR (eds) Seabird islands: ecology, invasion, and restoration. Oxford University Press, Oxford
91. Zelickman EA, Golovkin AN (1972) Composition, structure and productivity of neritic plankton communities near the bird colonies of the northern shores of Novaya Zemlya. Mar Biol 17:265-274