Abstract
Vertebrate consumers can be important drivers of the structure and functioning of ecosystems, including the soil and litter invertebrate communities that drive many ecosystem processes. Burrowing seabirds, as prevalent vertebrate consumers, have the potential to impact consumptive effects via adding marine nutrients to soil (i.e. resource subsidies) and non-consumptive effects via soil disturbance associated with excavating burrows (i.e. ecosystem engineering). However, the exact mechanisms by which they influence invertebrates are poorly understood. We examined how soil chemistry and plant and invertebrate communities changed across a gradient of seabird burrow density on two islands in northern New Zealand. Increasing seabird burrow density was associated with increased soil nutrient availability and changes in plant community structure and the abundance of nearly all the measured invertebrate groups. Increasing seabird densities had a negative effect on invertebrates that were strongly influenced by soil-surface litter, a positive effect on fungal-feeding invertebrates, and variable effects on invertebrate groups with diverse feeding strategies. Gastropoda and Araneae species richness and composition were also influenced by seabird activity. Generalized multilevel path analysis revealed that invertebrate responses were strongly driven by seabird engineering effects, via increased soil disturbance, reduced soil-surface litter, and changes in trophic interactions. Almost no significant effects of resource subsidies were detected. Our results show that seabirds, and in particular their non-consumptive effects, were significant drivers of invertebrate food web structure. Reductions in seabird populations, due to predation and human activity, may therefore have far-reaching consequences for the functioning of these ecosystems.
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi:10.1111/j.1442-9993.2001.01070ppx
Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268. doi:10.1890/02-0274
Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305:1955–1958. doi:10.1126/science.1101617
Borer ET, Seabloom EW, Tilman D (2012) Plant diversity controls arthropod biomass and temporal stability. Ecol Lett 15:1457–1464. doi:10.1111/ele.12006
Coomes DA, Allen RB, Scott NA, Goulding C, Beets P (2002) Designing systems to monitor carbon stocks in forests and shrublands. For Ecol Manag 164:89–108. doi:10.1016/S0378-1127(01)00592-8
Courchamp F, Chapuis J-L, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383. doi:10.1017/S1464793102006061
Crawley MJ (2007) The R book. Wiley, Chichester
Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV (2005) Introduced predators transform subarctic islands from grassland to tundra. Science 307:1959–1961. doi:10.1126/science.1108485
Croxall J, Butchart SH, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34
De Vries FT, Manning P, Tallowin JRB, Mortimer SR, Pilgrim ES, Harrison KA, Hobbs PJ, Quirk H, Shipley B, Cornelissen JHC, Kattge J, Bardgett RD (2012) Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecol Lett 15:1230–1239
Didham RK, Lawton JH, Hammond PM, Eggleton P (1998) Trophic structure stability and extinction dynamics of beetles (Coleoptera) in tropical forest fragments. Philos Trans R Soc Lond B 353:437–451
Doblas-Miranda E, Wardle DA, Peltzer DA, Yeates GW (2008) Changes in the community structure and diversity of soil invertebrates across the Franz Josef Glacier chronosequence. Soil Biol Biochem 40:1069–1081. doi:10.1016/j.soilbio.2007.11.026
Dunham AE (2008) Above and below ground impacts of terrestrial mammals and birds in a tropical forest. Oikos 117:571–579. doi:10.1111/j.0030-1299.2008.16534.x
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. doi:10.1007/s11258-005-7147-y
Fill A, Long EY, Finke DL (2012) Non-consumptive effects of a natural enemy on a non-prey herbivore population. Ecol Entomol 37:43–50. doi:10.1111/j.1365-2311.2011.01333.x
Freschet GT, Bellingham PJ, Lyver PO’B, Bonner KI, Wardle DA (2013) Plasticity in above- and belowground resource acquisition traits in response to single and multiple environmental factors in three tree species. Ecol Evol 3:1065–1078. doi:10.1002/ece3.520
Fukami T, Wardle DA, Bellingham PJ, Mulder CPH, Towns DR, Yeates GW, Bonner KI, Durrett MS, Grant-Hoffman MN, Williamson WM (2006) Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 9:1299–1307. doi:10.1111/j.1461-0248.2006.00983.x
Hall GMJ, Wiser SK, Allen RB, Beets PN, Goulding CJ (2001) Strategies to estimate national forest carbon stocks from inventory data: the 1990 New Zealand baseline. Glob Change Biol 7:389–403. doi:10.1046/j.1365-2486.2001.00419.x
Hendrix PF, Parmelee RW, Crossley DA Jr, Coleman DC, Odum EP, Groffman PM (1986) Detritus food webs in conventional and no-tillage agroecosystems. Bioscience 36:374–380. doi:10.2307/1310259
Hill JM, Weissburg MJ (2013) Predator biomass determines the magnitude of non-consumptive effects (NCEs) in both laboratory and field environments. Oecologia 172:79–91. doi:10.1007/s00442-012-2488-4
Ilmarinen K, Mikola J, Nieminen M, Vestberg M (2005) Does plant growth phase determine the response of plants and soil organisms to defoliation? Soil Biol Biochem 37:433–443. doi:10.1016/j.soilbio.2004.07.034
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386. doi:10.2307/3545850
Jonsson M, Yeates GW, Wardle DA (2009) Patterns of invertebrate density and taxonomic richness across gradients of area, isolation, and vegetation diversity in a lake-island system. Ecography 32:963–972. doi:10.1111/j.1600-0587.2009.05784.x
Kolb GS, Jerling L, Essenberg C, Palmborg C, Hambäck PA (2012) The impact of nesting cormorants on plant and arthropod diversity. Ecography 35:726–740. doi:10.1111/j.1600-0587.2011.06808.x
Kolb GS, Palmborg C, Hambäck PA (2013) Ecological stoichiometry and density responses of plant–arthropod communities on cormorant nesting islands. PLoS ONE 8:e61772. doi:10.1371/journal.pone.0061772
Kolb GS, Palmborg C, Taylor AR, Bååth E, Hambäck PA (2015) Effects of nesting cormorants (Phalacrocorax carbo) on soil chemistry, microbial communities, and soil fauna. Ecosystems 18:643–657. doi:10.1007/s10021-015-9853-1
Kramer M (2005) R2 statistics for mixed models. Proceedings of the Conference on Applied Statistics in Agriculture, Manhattan, KS, pp 148–160
Laliberté E, Tylianakis JM (2012) Cascading effects of long-term land-use changes on plant traits and ecosystem functioning. Ecology 93:145–155. doi:10.1890/11-0338.1
Loyola RD, Brito S-L, Ferreira RL (2006) Ecosystem disturbances and diversity increase: implications for invertebrate conservation. Biodivers Conserv 15:25–42. doi:10.1007/s10531-004-1870-x
Lyver PO’B (2000) Sooty shearwater (Puffinus griseus) harvest intensity and selectivity on Poutama Island, New Zealand. N Z J Ecol 24:169–180
Marczak LB, Thompson RM, Richardson JS (2007) Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–148. doi:10.1890/0012-9658(2007)88[140:MTLHAP]2.0.CO;2
Martin JEH (1977) Collecting, preparing and preserving insects, mites, and spiders. The insects and arachnids of Canada. Part 1. Publication 1643. Research Branch, Canada Department of Agriculture, Ottawa
McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Gleneden Beach
Mikola J, Setälä H, Virkajärvi P, Saarijärvi K, Ilmarinen K, Voigt W, Vestberg M (2009) Defoliation and patchy nutrient return drive grazing effects on plant and soil properties in a dairy cow pasture. Ecol Monogr 79:221–244. doi:10.1890/08-1846.1
Mulder CPH, Keall SN (2001) Burrowing seabirds and reptiles: impacts on seeds, seedlings and soils in an island forest in New Zealand. Oecologia 127:350–360. doi:10.1007/s004420000600
Mulder CPH, Jones HP, Kameda K, Palmborg C, Schmidt S, Ellis JC, Orrock JL, Wait DA, Wardle DA, Yang L, Young H, Croll DA, Vidal E (2011) Impacts of seabirds on plant and soil properties. In: Mulder CPH, Anderson WB, Towns DR, Bellingham PJ (eds) Seabird islands. Ecology, invasion and restoration. Oxford University Press, New York, pp 135–176
Nielsen UN, Osler GHR, van der Wal R, Campbell CD, Burslem DFRP (2008) Soil pore volume and the abundance of soil mites in two contrasting habitats. Soil Biol Biochem 40:1538–1541. doi:10.1016/j.soilbio.2007.12.029
Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, Bardgett RD (2010) Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–1083. doi:10.1111/j.1365-2745.2010.01679.x
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. doi:10.1086/285858
Polis GA, Hurd SD, Jackson CT, Sanchez-Piñero F (1998) Multifactor population limitation: variable spatial and temporal control of spiders on Gulf of California islands. Ecology 79:490–502. doi:10.2307/176948
R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org
Sánchez-Piñero F, Polis GA (2000) Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81:3117–3132. doi:0.2307/177405
Sanders D, Jones CG, Thébault E, Bouma TJ, van der Heide T, van Belzen J, Barot S (2014) Integrating ecosystem engineering and food webs. Oikos 123:513–524. doi:10.1111/j.1600-0706.2013.01011.x
Schaffers AP, Raemakers IP, Sýkora KV, ter Braak CJF (2008) Arthropod assemblages are best predicted by plant species composition. Ecology 89:782–794. doi:10.1890/07-0361.1
Schmitz OJ, Grabowski JH, Peckarsky BL, Preisser EL, Trussell GC, Vonesh JR (2008) From individuals to ecosystem function: toward an integration of evolutionary and ecosystem ecology. Ecology 89:2436–2445. doi:10.1890/07-1030.1
Schmitz OJ, Hawlena D, Trussell GC (2010) Predator control of ecosystem nutrient dynamics. Ecol Lett 13:1199–1209. doi:10.1111/j.1461-0248.2010.01511.x
Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368. doi:10.1890/08-1034.1
Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070. doi:10.2307/176709
Smith JL, Mulder CPH, Ellis JC (2011) Seabirds as ecosystem engineers: nutrient inputs and physical disturbance. In: Mulder CPH, Anderson WB, Towns DR, Bellingham PJ (eds) Seabird islands. Ecology, invasion, and restoration. Oxford University Press, New York, pp 27–54
St. John MG, Crossley DA Jr, Coleman DC (2012) Microarthropods. In: Huang PM, Li YC, Sumner ME (eds) Handbook of soil sciences: resource management and environmental impacts, vol 1, 2nd edn. Taylor & Francis, Boca Raton
Towns DR (2002) Korapuki island as a case study for restoration of insular ecosystems in New Zealand. J Biogeogr 29:593–607. doi:10.1046/j.1365-2699.2002.00709.x
Towns DR, Wardle DA, Mulder CPH, Yeates GW, Fitzgerald BM, Parrish GR, Bellingham PJ, Bonner KI (2009) Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118:420–430. doi:10.1111/j.1600-0706.2008.17186.x
Uetz GW (1991) Habitat structure and spider foraging. In: McCoy ED, Bell SS, Mushinsky HR (eds) Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London, pp 325–348. doi: 10.1007/978-94-011-3076-9_16
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. doi:10.1016/j.jaridenv.2004.07.001
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton
Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886. doi:10.1111/j.1461-0248.2006.00931.x
Wardle DA, Yeates GW, Barker GM, Bonner KI (2006) The influence of plant litter diversity on decomposer abundance and diversity. Soil Biol Biochem 38:1052–1062. doi:10.1016/j.soilbio.2005.09.003
Wardle DA, Bellingham PJ, Bonner KI, Mulder CPH (2009) Indirect effects of invasive predators on litter decomposition and nutrient resorption on seabird-dominated islands. Ecology 90:452–464. doi:10.1890/08-0097.1
Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55:25–38. doi:10.1111/j.1744-7348.1965.tb07864.x
Whitehead AL, Lyver PO’B, Jones CJ, Bellingham PJ, MacLeod CJ, Coleman M, Karl BJ, Drew K, Pairman D, Gormley AM, Duncan RP (2014) Establishing accurate baseline estimates of breeding populations of a burrowing seabird, the grey-faced petrel (Pterodroma macroptera gouldi) in New Zealand. Biol Conserv 169:109–116. doi:10.1016/j.biocon.2013.11.002
Wimp GM, Murphy SM, Finke DL, Huberty AF, Denno RF (2010) Increased primary production shifts the structure and composition of a terrestrial arthropod community. Ecology 91:3303–3311. doi:10.1890/09-1291.1
Zmudeczyńska-Skarbek K, Barcikowski M, Zwolicki A, Iliszko L, Stempniewicz L (2013) Variability of polar scurvygrass Cochlearia groenlandica individual traits along a seabird influenced gradient across Spitsbergen tundra. Polar Biol 36:1659–1669. doi:10.1007/s00300-013-1385-6
Acknowledgments
We thank members of the Ruamāhua Islands Trust, Hauraki Collective, Ngāti Hei Trust, and Ngāti Whānaunga, for their support and approval to access Ruamāhuanui and Korapuki islands. The scientific and logistical support of staff from the Department of Conservation Thames Area Office was appreciated. We thank Morgan Coleman, Keven Drew, Brian Karl, Caroline Thomson, Lindsay Smith, Karen Boot, Neil Fitzgerald, Jenny Hurst, Chris Morse and Kate Ladley (Landcare Research), Ewen Cameron (Auckland Museum), David Hamon and Frank Waitai (Hauraki) for field assistance. We acknowledge the service of our charter operators Waters Edge Charters (Whitianga) and Skyworks Helicopters. We also thank Duane Peltzer and Sarah Richardson (Landcare Research) for help with statistics. This project was funded primarily by New Zealand’s Ministry of Business, Innovation and Employment’s Mauriora ki nga Oi (Safe-guarding the life force of the grey-faced petrel—C09X0509) and Te Hiringa Tangata Ki Tai Pari Ki Tai Timu (Bicultural restoration of coastal forest ecosystems—C09X0908) projects. D.R.T. received funding assistance from the Department of Conservation and D.W. was supported by a Wallenberg Scholars award.
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CJ, DAW, DRT, PJB, PO’BL formulated the idea. CJ, DAW, DRT, PJB, MGStJ, PO’BL designed the experiment. PJB, MGStJ, BMF, RGP, DRT collected the data. KHO analyzed the data. KHO, DAW, DRT, MGStJ and PJB wrote the manuscript; other authors provided editorial advice and expertise for invertebrate identification.
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Communicated by Volkmar Wolters.
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442_2015_3437_MOESM1_ESM.pdf
ESM: Online Resource 1:Photos of example plots of different seabird burrow density. Online Resource 2: Maps of islands and location of plots. Online Resource 3: Variables used in the PCA analyses summarising prey abundance and soil chemistry. Online Resource 4: Effects of burrow density and island on PCA scores. Online Resource 5: Effects of burrow density and island on PCA scores calculated for Araneae analyses. Online Resource 6: Effect of burrow density on litter and soil chemistry. Online Resource 7: Results from PCA analysis of tree species composition. Online Resource 8: Effect of burrow density on invertebrate abundance and species richness. Online Resource 9: Results from PCA analysis of Gastropoda species composition. Online Resource 10: Results from PCA analysis of Araneae species composition. Online Resource 11: Effect of island identity on the response variables measured. Online Resource 12: Estimates of model fit for the final generalized multilevel path models. (PDF 1677 kb)
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Orwin, K.H., Wardle, D.A., Towns, D.R. et al. Burrowing seabird effects on invertebrate communities in soil and litter are dominated by ecosystem engineering rather than nutrient addition. Oecologia 180, 217–230 (2016). https://doi.org/10.1007/s00442-015-3437-9
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DOI: https://doi.org/10.1007/s00442-015-3437-9