The transport of nutrients by migratory animals across ecosystem boundaries can significantly enrich recipient food webs, thereby shaping the ecosystems’ structure and function. To illustrate the potential role of islands in enabling the transfer of matter across ecosystem boundaries to be gauged, we investigated the influence of seabirds on nitrogen input on islands. Basing our study on four widely differing islands in terms of their biogeography and ecological characteristics, sampled at different spatial and temporal intervals, we analyzed the nitrogen isotopic values of the main terrestrial ecosystem compartments (vascular plants, arthropods, lizards and rodents) and their relationship to seabird values. For each island, the isotopic values of the ecosystem were driven by those of seabirds, which ultimately corresponded to changes in their marine prey. First, terrestrial compartments sampled within seabird colonies were the most enriched in δ15N compared with those collected at various distances outside colonies. Second, isotopic values of the whole terrestrial ecosystems changed over time, reflecting the values of seabirds and their prey, showing a fast turnover throughout the ecosystems. Our results demonstrate that seabird-derived nutrients not only spread across the terrestrial ecosystems and trophic webs, but also modulate their isotopic values locally and temporally on these islands. The wealth of experimental possibilities in insular ecosystems justifies greater use of these model systems to further our understanding of the modalities of trans-boundary nutrient transfers.
References
[1]
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Evol S 28: 289–316.
[2]
Sanchez-Pi？ero F, Polis GA (2000) Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81: 3117–3132.
[3]
Stapp PG, Polis GA (2003) Influence of pulsed resources and marine subsidies on insular rodent populations. Oikos 102: 111–123.
[4]
Ellis JC, Farina JM, Witman JD (2006) Nutrient transfer from sea to land: the case of gulls and cormorants in the Gulf of Maine. J Anim Ecol 75: 565–574.
[5]
Michelutti N, Keatley BE, Brimble S, Blais JM, Liu H, et al. (2009) Seabird-driven shifts in Arctic pond ecosystems. Proc R Soc Lond B 276: 591–596.
[6]
Farina JM, Salazar S, Wallem KP, Witman JD, Ellis JC (2003) Nutrient exchanges between marine and terrestrial ecosystems: the case of the Galapagos sea lion Zalophus wollebaeki. J Anim Ecol 72: 873–887.
[7]
Hilderbrand GV, Hanley TA, Robbins CT, Schwartz CC (1999) Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem. Oecologia 121: 546–550.
[8]
Bouchard SS, Bjorndal KA (2000) Sea turtles as biological transporters of nutrients and energy from marine to terrestrial ecosystems. Ecology 81: 2305–2313.
Blais JM, MacDonald RW, MacKay D, Webster E, Harvey C, et al. (2007) Biologically mediated transport of contaminants to aquatic systems. Int J Environ Sci Technol 41: 1075–1084.
[11]
Carlton JT, Hodder J (2003) Maritime mammals: terrestrial mammals as consumers in marine intertidal communities. Mar Ecol Prog Ser 256: 271–286.
[12]
Sun LG, Xie ZQ, Zhao JL (2000) A 3,000-years record of penguin populations. Nature 407: 858.
[13]
Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV (2005) Introduced predators transform subarctic islands from grassland to tundra. Science 307: 1959–1961.
[14]
Mulder CPH, Anderson WB, Towns DR, Bellingham PJ (2011) Seabird islands: ecology, invasion and restoration. Oxford University Press, 492 pp.
[15]
Kelly JK (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78: 1–27.
[16]
Anderson WB, Polis GA (1999) Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia 118: 324–332.
[17]
Mizutani H, Kabaya Y, Wada E (1985) Ammonia volatilization and high 15N/14N ratio in a penguin rookery in Antarctica. Geochem J 19: 323–327.
[18]
Powell GVN, Fourqurean JW, Kenworthy WJ, Zieman JC (1991) Bird colonies cause seagrass enrichment in a subtropical estuary: observational and experimental evidence. Estuar Coast Shelf S 32: 567–579.
[19]
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.
[20]
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.
[21]
Ellis JC (2005) Marine birds on land: a review of plant biomass, species richness and community composition in seabird colonies. Plant Ecol 181: 227–241.
[22]
Markwell TJ, Daugherty CH (2002) Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience 9: 293–299.
[23]
Anderson WB, Wait DA, Stapp P (2008) Resources from another place and time: responses to pulses in a spatially subsidized system. Ecology 89: 660–670.
[24]
Stapp PG, Polis GA, Pi？ero FS (1999) Stable isotopes reveal strong marine and El Nino effects on island food webs. Nature 401: 467–469.
[25]
Fukami T, Wardle DA, Bellingham PJ, Mulder CP, Towns DR, et al. (2006) Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 9: 1299–307.
[26]
Wardle DA, Bellingham PJ, Fukami T, Mulder CPH (2007) Promotion of ecosystem carbon sequestration by invasive predators. Biol Lett 3: 479–482.
[27]
Mulder CPH, Nicole Grant-Hoffman M, Towns DR, Bellingham PJ, Wardle DA, et al. (2009) Direct and indirect effects of rats: does rat eradication restore ecosystem functioning of New Zealand seabird islands? Biol Invasions 11: 1671–1688.
[28]
Pascal M, Lorvelec O, Pisanu B, Chapuis J-L, Vidal E (2009) L’élaboration progressive d’une stratégie d’éradication adaptée à une population micro insulaire de rongeurs aux Iles Marquises. Te Manu 65: 6–9.
[29]
Pisanu B, Caut S, Gutjahr S, Vernon P, Chapuis J-L (2011) Introduced black rats Rattus rattus on Ile de la Possession (Iles Crozet, Subantarctic): diet and trophic position in food webs. Pol Biol 34: 169–180.
[30]
Ruffino L, Russell JC, Pisanu B, Caut S, Vidal E (2011) Low individual-level diet plasticity in an island-invasive generalist forager. Pop Ecol 53: 535–548.
[31]
Caut S, Angulo E, Courchamp F (2009) Avoiding surprise effects on Surprise Island: alien species control in a multitrophic level perspective. Biol Invasions 11: 1689–1703.
[32]
Rosenthal R, Rosnow RL (1985) Contrast analysis: focused comparisons in the analysis of variance. Cambridge University Press, Cambridge, UK.
[33]
SAS Institute Inc (2004) SAS, 9.1.3, Help and Documentation. SAS Institute Inc., Cary; N.C, USA.
[34]
Mizutani H, Wada E (1988) Nitrogen and carbon isotope ratios in seabird rookeries and their ecological implications. Ecology 69: 340–349.
[35]
Polis GA, Hurd SD (1996) Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat 147: 396–423.
[36]
Maron JL, Estes JA, Croll DA, Danner EM, Elmendorf SC, et al. (2006) An introduced predator alters Aleutian island plant communities by thwarting nutrient subsidies. Ecol Monogr 76: 3–24.
[37]
Mulder CPH, Jones HP, Kameda K, Palmborg C, Schmidt S, et al. (2011) Impacts of seabirds on plant and soil properties. In CPH Mulder, et al. (eds) Seabird islands: ecology, invasion and restoration. Oxford University Press, 492 pp.
[38]
Orgeas J, Vidal E, Ponel P (2003) Colonial seabirds change beetle assemblages on a Mediterranean island. Ecoscience 10: 38–44.
[39]
Barrett K, Anderson WB, Wait DA, Grismer LL, Polis GA, et al. (2005) Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos 109: 145–153.
[40]
Kolb GS, Young HS, Anderson WB (2011) Effects of seabirds on island consumers. In CPH Mulder, et al. (eds) Seabird islands: ecology, invasion and restoration. Oxford University Press, 492 pp.
[41]
Beerling DJ (2011) Quantitative estimates of changes in marine and terrestrial primary productivity over the past 300 million years. Proc R Soc Lond B 266: 1821–1827.
[42]
Whittaker RH (1961) Experiments with radiophosphorus tracer in aquarium microcosms. Ecol Monogr 31: 157–188.
[43]
Erskine PD, Bergstrom DM, Schmidt S, Stewart GR, Tweedie CE, et al. (1998) Subantarctic Macquarie island – a model ecosystem for studying animal-derived nitrogen sources using 15N natural abundance. Oecologia 117: 187–193.
[44]
Lindeboom HJ (1984) The nitrogen pathway in a penguin rookery. J Ecol 65: 269–277.
[45]
Schmidt S, Dennison WC, Moss GJ, Stewart GR (2004) Nitrogen of Heron Island, a subtropical coral cay of the Great Barrier Reef, Australia. Funct Plant Biol 31: 517–528.
[46]
Wait DA, Aubrey DP, Anderson WB (2005) Seabird guano influences on desert islands: soil chemistry and herbaceous species richness and productivity. J Arid Environ 60: 681–695.
[47]
Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8: 863–891.
[48]
Sekercioglu CH, Daily GC, Ehrlich PR (2004) Ecosystem consequences of bird declines. P Natl Acad Sci USA 101: 18042–18047.
[49]
Vidal E, Medail F, Tatoni T, Roche P, Vidal P (1998) Impact of gull colonies on the flora of the Riou Archipelago (Mediterranean islands of south-east France). Biol Conserv 84: 235–243.
[50]
Vidal E, Medail F, Tatoni T, Bonnet V (2000) Seabirds drive plant species turnover on small Mediterranean islands at the expense of native taxa. Oecologia 122: 427–434.
[51]
Kolb A, Alpert P, Enters D, Holzapfed C (2002) Patterns of invasion within a grassland community. J Ecol 90: 871–881.
[52]
Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40: 344–53.
[53]
Finney SK, Harris MP, Keller LF, Elston DA, Monaghan P, et al. (2003) Reducing the density of breeding gulls influences the pattern of recruitment of immature Atlantic puffins Fratercula artica to a breeding colony. J Appl Ecol 40: 545–552.
