Abstract
This study examined the recovery, via biotic and abiotic pathways, of a grassland ecosystem after eradication of introduced exotic goats. We used path analyses to evaluate the relative strength of relationships among aboveground biomass, soil chemical properties (carbon, nitrogen, and phosphorus content; soil acidity), presence of nesting seabirds after goat eradication, extent of vegetation degraded by goats before their eradication, plant species composition after removal of goats, and topography. Models including the same variables with different paths were constructed using the Bayesian estimation method, and the best-fit models were constructed by comparing deviance information criterion values. Results of the path analyses demonstrated that vegetation degradation and soil erosion prior to goat eradication increased soil exchangeable acidity, which resulted in limitation of aboveground biomass. Seabird nesting after goat eradication increased the quantity of soil nutrients, possibly through inputs of feces, eggshells, and dead chicks or adults. The increase in nutrients was affected indirectly, via seabird nesting, by topography and vegetation type after goat eradication. The direct and indirect relationships demonstrated by our results suggest the existence of complex interrelationships during recovery of ecosystem function after eradication of exotic mammals.
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References
Anderson WB, Polis GA. 1999. Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia 118:324–32.
Anderson WB, Wait DA, Stapp P. 2008. Resources from another place and time: responses to pulses in a spatially subsidized system. Ecology 89:660–70.
Aoyama, Y. 2013. Alien mammal impacts on seabird populations and seabird impacts on flora in the Ogasawara Islands. PhD thesis, Tohoku University, Miyagi, Japan.
Bardgett R. 2005. The biology of soil: a community and ecosystem approach. Oxford, UK: Oxford University Press. p 256.
Bergstrom DM, Lucieer A, Kiefer K, Wasley J, Belbin L, Pedersen TK, Chown SL. 2009. Indirect effects of invasive species removal devastate World Heritage Island. J Appl Ecol 46:73–81.
Brodier S, Pisanu B, Villers A, Pettex E, Lioret M, Chapuis J-L, Bretagnolle V. 2011. Responses of seabirds to the rabbit eradication on Ile Verte, sub-Antarctic Kerguelen Archipelago. Anim Conserv 14:459–65.
Campbell KJ, Donlan CJ. 2005. A review of feral goat eradication on islands. Conserv Biol 19:1362–74.
Carrion V, Donlan CJ, Campbell K, Lavoie C, Cruz F. 2007. Feral donkey (Equus asinus) eradications in the Galápagos. Biodivers Conserv 16:437–45.
Chiba H, Kawakami K, Suzuki H, Horikoshi K. 2007. The distribution of seabirds in the Bonin Islands, Southern Japan. J Yamashina Inst Ornithol 39:1–17.
Courchamp F, Chapuis J-L, Pascal M. 2003. Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–83.
Donlan CJ, Wilcox C. 2008. Integrating invasive mammal eradications and biodiversity offsets for fisheries by catch: conservation opportunities and challenges for seabirds and sea turtles. Biol Invasions 10:1053–60.
Ellis JC, Fariña JM, Jon Witman JD. 2006. Nutrient transfer from sea to land: the case of gulls and cormorants in the Gulf of Maine. J Anim Ecol 75:565–74.
Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Ann Rev Ecol Evol Syst 35:557–81.
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 9:1299–307.
Gelman A, Carlin JB, Stern HS, Rubin DB. 2004. Bayesian data analysis. London, UK: CRC Press.
Golluscio RA, Austin AT, Martínez GCG, Gonzalez-Polo M, Sala OE, Jackson RB. 2009. Sheep grazing decreases organic carbon and nitrogen pools in the Patagonian steppe: combination of direct and indirect effects. Ecosystems 12:686–97.
Grant-Hoffman MN, Mulder CP, Bellingham PJ. 2010a. Invasive rats alter woody seedling composition on seabird-dominated islands in New Zealand. Oecologia 163:449–60.
Grant-Hoffman MN, Mulder CPH, Bellingham PJ. 2010b. Effects of invasive rats and burrowing seabirds on seeds and seedlings on New Zealand islands. Oecologia 162:1005–16.
Harris DB, Macdonald DW. 2007. Interference competition between introduced black rats and endemic Galapagos rice rats. Ecology 88:2330–44.
Hata K, Kachi N, Ichikawa S. 2003. Vegetation changes in the Nakoudojima Island after goat eradication. Ann Rep Ogasawara Res 26:39–46 (in Japanese).
Hata K, Suzuki J-I, Kachi N. 2007. Vegetation changes between 1978, 1991 and 2003 in the Nakoudojima island that had been disturbed by feral goats. Ogasawara Res 32:1–8.
Hata K, Kachi N. 2012. Nine yeas changes in herbaceous vegetation on the Nakoudojima Island after goat eradication. Ann Rep Ogasawara Res 35:23–8 (in Japanese).
Hata K, Kohri M, Morita S, Hiradate S, Kachi N. Fine-scale distribution of aboveground biomass of herbaceous vegetation and soil nutrients on an oceanic island after goat eradication are correlated with grazing damage and seabird nesting. Pac Conserv Biol in press.
Hiradate S, Ma JF, Matsumoto H. 2007. Strategies of plants to adapt to mineral stresses in problem soils. Adv Agron 96:65–132.
Hoyo JD, Elliott A, Sargatel J. 1992. Ostrich to Ducks. In: Handbook of the birds of the world, Vol. 1. Barcelona: Lynx Edicions.
Ishida A. 1996. Effects of the common cormorant, Phalacrocorax carbo, on evergreen forests in two nest sites at Lake Biwa, Japan. Ecol Res 112:193–200.
Japan Wildlife Research Center. 1992. Report on the urgent research about damage of feral goats on plants and animals in the Ogasawara Islands. Japan Wildlife Research Center, Tokyo, Japan. (in Japanese).
Japan Wildlife Research Center. 2002. Report on the research of vegetation recovery in the Ogasawara National Park. Ogasawara branch of Tokyo Metropolitan Government, Tokyo, Japan. (in Japanese).
Japan Wildlife Research Center. 2012. Report on the research of vegetation recovery in the Ogasawara National Park. Ogasawara branch of Tokyo Metropolitan Government, Tokyo, Japan. (In Japanese).
Jones HP. 2010a. Seabird islands take mere decades to recover following rat eradication. Ecol Appl 20:2075–80.
Jones HP. 2010b. Prognosis for ecosystem recovery following rodent eradication and seabird restoration in an island archipelago. Ecol Appl 20:1204–16.
Kawakami K, Suzuki H, Chiba H, Horikoshi K. 2008. Avifauna of Minami-Iwo-To Island, Volcano Islands, the Bonin Islands. Ogasawara Res 33:111–27 (In Japanese with English abstract).
Loope LL, Hamann O, Stone CP. 1988. Comparative conservation biology of oceanic archipelagoes: Hawaii and the Galapagos. BioSci 38:272–82.
Morita S, Kato H, Iwasaki N, Kusumoto Y, Yoshida K, Hiradate S. 2010. Unusually high levels of bio-available phosphate in the soils of Ogasawara Islands, Japan, Putative influence of seabirds. Geoderma 160:155–64.
Mulder CPH, Grant-Hoffman MN, Towns DR, Bellingham PJ, Wardle DA, Durrett MS, Fukami T, Bonner KI. 2009. Direct and indirect effects of rats: does rat eradication restore ecosystem functioning of New Zealand seabird islands? Biol Invasions 11:1671–88.
Murphy J, Riley JP. 1962. A modified single solution method for determination of phosphate in natural waters. Anal Chim Acta 27:31–6.
Peay KG, Dickie IA, Wardle DA, Bellingham PJ, Fukami T. 2013. Rat invasion of islands alters fungal community structure, but not wood decomposition rates. Oikos 122:258–64.
Rayner MJ, Hauber ME, Imber MJ, Stamp RK, Clout MN. 2007. Spatial heterogeneity of mesopredator release within an oceanic island system. Proc Natl Acad Sci USA 104:20862–5.
Roverts CM, Duncan RP, Wilson KJ. 2007. The effects of burrowing seabirds on forest regeneration, Rangatira Island, Chatham Islands, New Zealand. New Zeal J Ecol 31:208–22.
Saigusa M, Shoji S, Takahashi T. 1980. Plant root growth in acid Andosols from northeastern Japan: 2. Exchange acidity Y1 as a realistic measure of aluminum toxicity potential. Soil Sci 130:242–50.
Shimizu Y. 1993. Vegetation of Mukojima Island Group in the Bonin (Ogasawara) Islands with reference to the ecology of Ardisia dominant forest and the influence of feral goats. Komazawa Geogr 29:9–58 (in Japanese).
Steffens M, Kölbl A, Totsche KU, Kögel-Knabner I. 2008. Grazing effects on soil chemical and physical properties in a semiarid steppe of Inner Mongolia (PR China). Geoderma 143:63–72.
Suding KN, Gross KL, Houseman GR. 2004. Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53.
Towns DR, Wardle DA, Mulder CPH, Yeates GW, Fitzgerald BM, Richard Parrish G, Bellingham PJ, Bonner KI. 2009. Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118:420–30.
Vitousek PM. 2002. Oceanic islands as model systems for ecological studies. J Biogeogr 29:573–82.
Wardle DA. 2002. Islands as model systems for understanding how species affect ecosystem properties. J Biogeogr 29:583–91.
Wardle DA, Bellingham PJ, Fukami T, Bonner KI. 2012. Soil-mediated indirect impacts of an invasive predator on plant growth. Biol Lett 8:574–7.
Wootton JT. 1994. Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–65.
Yong-Zhong S, Yu-Lin L, Jian-Yuan C, Wen-Zhi Z. 2005. Influences of continuous grazing and livestock exclusion on soil properties in a degraded sandy grassland, Inner Mongolia, northern China. Catena 59:267–78.
Acknowledgments
We thank the Ministry of Environment and the Department of National Forests in the Ogasawara Islands for allowing us to conduct this study. This work was partly supported by JSPS KAKENHI Grant Number 22241055 and 24710274. Drs. Kazuto Kawakami, Katsuhiko Yoshida, and Yukiko Aoyama provided valuable information for discussion in this study. Dr. Kyoko Sugai helped in the field and with species identification. Drs. Taisuke Yasuda, Satoshi N. Suzuki, and Keita Fukasawa provided useful information about statistical analyses. Two anonymous reviewers and the subject-matter editor made numerous valuable comments that improved this manuscript.
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Kenji Hata, Syuntaro Hiradate, Naoki Kachi conceived of or designed study. Kenji Hata, Sayaka Morita, Syuntaro Hiradate performed field research. Sayaka Morita, Syuntaro Hiradate analyzed soil chemical properties. Kenji Hata, Mari Kohri analyzed data. Kenji Hata, Mari Kohri, Sayaka Morita, Syuntaro Hiradate, Naoki Kachi wrote the paper
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Hata, K., Kohri, M., Morita, S. et al. Complex Interrelationships Among Aboveground Biomass, Soil Chemical Properties, and Events Caused by Feral Goats and Their Eradication in a Grassland Ecosystem of an Island. Ecosystems 17, 1082–1094 (2014). https://doi.org/10.1007/s10021-014-9780-6
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DOI: https://doi.org/10.1007/s10021-014-9780-6