Biological Invasions

, Volume 11, Issue 7, pp 1671–1688 | Cite as

Direct and indirect effects of rats: does rat eradication restore ecosystem functioning of New Zealand seabird islands?

  • Christa P. H. Mulder
  • M. Nicole Grant-Hoffman
  • David R. Towns
  • Peter J. Bellingham
  • David A. Wardle
  • Melody S. Durrett
  • Tadashi Fukami
  • Karen I. Bonner
Invasive Rodents on Islands


Introduced rats (Rattus spp.) can affect island vegetation structure and ecosystem functioning, both directly and indirectly (through the reduction of seabird populations). The extent to which structure and function of islands where rats have been eradicated will converge on uninvaded islands remains unclear. We compared three groups of islands in New Zealand: islands never invaded by rats, islands with rats, and islands on which rats have been controlled. Differences between island groups in soil and leaf chemistry and leaf production were largely explained by burrow densities. Community structure of woody seedlings differed by rat history and burrow density. Plots on islands with high seabird densities had the most non-native plant species. Since most impacts of rats were mediated through seabird density, the removal of rats without seabird recolonization is unlikely to result in a reversal of these processes. Even if seabirds return, a novel plant community may emerge.


Invasive plants Rat eradication Restoration Seabird density Soil characteristics Woody seedlings 



For permission to work on the islands they own or for which they are kaitiaki (guardians), we thank the following iwi: Ngāti Hako, Ngāti Hei, Ngāti Manuhiri, Ngāti Paoa, Ngāti Puu, Ngāti Rehua, and Ngātiwai, as well as the Ruamāhua (Aldermen) Islands Trust, the Ngamotuaroha Trust, John McCallum, Oho Nicolls, Bryce Rope, and the Neureuter family. We thank the New Zealand Department of Conservation for facilitating our visits to the islands they administer. We also thank Larry Burrows, Ewen Cameron, Ellen Cieraad, Brian Daly, Aaron Hoffman, Holly Jones, Brian Karl, Rau Kirikiri, Nora Leipner, Phil Lyver, Richard Parrish, Gaye Rattray, James Russell, and Dan Uliassi for assistance. The comments of two anonymous reviewers improved the manuscript. This study was supported by the Marsden Fund of the Royal Society of New Zealand, the U.S. National Science Foundation (DEB-0317196), the New Zealand Foundation for Research, Science and Technology (Sustaining and restoring biodiversity OBI), the New Zealand Department of Conservation, and the Japan Society for the Promotion of Science.


  1. Allen RB, Lee WG, Rance BD (1994) Regeneration in indigenous forest after eradication of Norway rats, Breaksea Island, New Zealand. New Zeal J Bot 32:429–439Google Scholar
  2. Anderson WB, Polis GA (1999) Nutrient fluxes from water to land: seabirds affect plant quality on Gulf of California islands. Oecologia 118:324–332CrossRefGoogle Scholar
  3. Anderson WB, Wait DA (2001) Subsidized island biogeography hypothesis: a new twist on an old theory. Ecol Lett 4:289–291CrossRefGoogle Scholar
  4. Atkinson IAE (1985) The spread of commensal species of Rattus to oceanic islands and their effects on island avifauna. In: Moors PJ (ed) Conservation of Island Birds. ICBP technical publication no. 3. ICBP, Cambridge, pp 35–81Google Scholar
  5. Atkinson IAE (2004) Successional processes induced by fires on the northern offshore islands of New Zealand. New Zeal J Ecol 28:181–194Google Scholar
  6. Bancroft WJ, Garkaklis MJ, Roberts JD (2005a) Burrow building in seabird colonies: a soil-forming process in island ecosystems. Pedobiologia 49:149–165CrossRefGoogle Scholar
  7. Bancroft WJ, Roberts JD, Garkaklis MJ (2005b) Burrowing seabirds drive decreased diversity and structural complexity, and increased productivity in insular-vegetation communities. Aust J Bot 53:231–241CrossRefGoogle Scholar
  8. Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305:1955–1958PubMedCrossRefGoogle Scholar
  9. Blakemore LC, Gibbs HS (1968) Effects of gannets on soil at Cape Kidnappers, Hawke’s Bay. New Zeal J Sci 11:54–62Google Scholar
  10. Blakemore LC, Searle PL, Daly BK (1987) Methods for chemical analysis of soils. New Zealand Soil Bureau Scientific Report 80Google Scholar
  11. Bremner AG, Butcher CF, Patterson GB (1984) The density of indigenous invertebrates on three islands in Breaksea Sound, Fiordland, in relation to the distribution of introduced mammals. J R Soc New Zeal 14:379–386Google Scholar
  12. Broadhurst RB, Jones WT (1978) Analysis of condensed tannins using acidified vanillin. J Sci Food Agric 29:788–794CrossRefGoogle Scholar
  13. Burbidge AA, Manly BFJ (2002) Mammal extinctions on Australian islands: causes and conservation implications. J Biogeog 29:465–473CrossRefGoogle Scholar
  14. Burger AE (2005) Dispersal and germination of seeds of Pisonia grandis, an Indo–Pacific tropical tree associated with insular seabird colonies. J Trop Ecol 21:263–271CrossRefGoogle Scholar
  15. Campbell DJ, Atkinson IAE (1999) Effects of kiore (Rattus exulans Peale) on recruitment of indigenous coastal trees on northern offshore islands of New Zealand. J R Soc New Zeal 29:265–290Google Scholar
  16. Campbell DJ, Atkinson IAE (2002) Depression of tree recruitment by the Pacific rat (Rattus exulans Peale) on New Zealand’s northern offshore islands. Biol Conserv 107:19–35CrossRefGoogle Scholar
  17. Caut S, Angulo E, Courchamp F (2008) Avoiding surprise effects on Surprise Island: alien species control in a multitrophic level perspective. Biol Invasions. doi: 10.1007/s10530-008-9397-9 Google Scholar
  18. Cree A, Daugherty CH, Hay JM (1995) Reproduction of a rare New Zealand reptile, the tuatara Sphenodon punctatus on rat-free and rat-inhabited islands. Conserv Biol 9:373–383CrossRefGoogle Scholar
  19. D’Antonio CM, Dudley TL, Mack M (1999) Disturbance and biological invasions: direct effects and feedbacks. In: Walker LR (ed) Ecosystems of disturbed ground. Elsevier, Amsterdam, pp 413–452Google Scholar
  20. Delgado Garcia JD (2000) Selection and treatment of fleshy fruits by the ship rat (Rattus rattus L.) in the Canarian laurel forest. Mammalia 64:11–18CrossRefGoogle Scholar
  21. Ellis JC (2005) Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol 181:227–241CrossRefGoogle Scholar
  22. 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 9:1299–1307PubMedCrossRefGoogle Scholar
  23. Furness RW (1991) The occurrence of burrow-nesting among birds and its influence on soil fertility and stability. In: Meadows PS, Meadows A (eds) The environmental impact of burrowing animals and animal burrows. Oxford University Press, Oxford, pp 53–67Google Scholar
  24. Gaze P (2000) The response of a colony of sooty shearwater (Puffinus griseus) and flesh-footed shearwater (P. carneipus) to the cessation of harvesting and the eradication of Norway rats (Rattus norvegicus). New Zeal J Zool 27:375–379Google Scholar
  25. Gaze P (2001) Tuatara recovery plan 2001–2011. Threatened species recovery plan 47. Department of Conservation, WellingtonGoogle Scholar
  26. Gillham ME (1956a) Ecology of the Pembrokeshire Islands V. Manuring by seabirds and mammals, with a note on seed distribution by gulls. J Ecol 44:429–454CrossRefGoogle Scholar
  27. Gillham ME (1956b) Ecology of the Pembrokeshire Islands IV. Effects of treading and burrowing by birds and mammals. J Ecol 44:51–82CrossRefGoogle Scholar
  28. Graham MF, Veitch CR (2002) Changes in bird numbers on Tiritiri Matangi island, New Zealand, over the period of rat eradication. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species IUCN invasive species specialist group. IUCN, Gland, pp 413–452Google Scholar
  29. Howald G, Donland CJ, Galván JB, Russell JC, Parkes J, Samaniego A, Wang Y, Veitch D, Genovesi P, Pascal M, Saunders A, Tershy B (2007) Invasive rodent eradications on islands. Conserv Biol 21:1258–1268PubMedCrossRefGoogle Scholar
  30. Imber M, Harrison M, Harrison J (2000) Interactions between petrels, rats and rabbits on Whale Island, and effects of rat and rabbit eradication. New Zeal J Ecol 24:153–160Google Scholar
  31. Jones HP, Tershy BR, Zavaleta ES, Croll DA, Keitt BS, Finkelstein ME, Howald GR (2008) Review of the global severity of the effects of invasive rats on seabirds. Conser Biol 22:16–26CrossRefGoogle Scholar
  32. Kress SW (1983) The use of decoys, sound recordings, and gull control for re-establishing a tern colony in Maine. Colon Waterbird 6:185–196CrossRefGoogle Scholar
  33. Maesako Y (1991) Effects of streaked shearwater Calonectris leucomelas on species composition of Persea thunbergii forest on Kanmurijima Island, Kyoto Prefecture, Japan. Ecol Res 6:371–378CrossRefGoogle Scholar
  34. Magurran AE (1988) Ecological diversity and its measurement. Princeton Uni Press, PrincetonGoogle Scholar
  35. Marchant S, Higgins PJ (1990) Australian, New Zealand, and Antarctic Birds. Volume 1 ratites to ducks. Oxford University Press, MelbourneGoogle Scholar
  36. 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. Écoscience 9:293–299Google Scholar
  37. McAlpine K, Drake DR (2003) The effects of small-scale environmental heterogeneity on seed germination in experimental treefall gaps in New Zealand. Plant Ecol 165:207–215CrossRefGoogle Scholar
  38. McConkey KR, Drake DR, Meehan HJ, Parsons N (2003) Husking stations provide evidence of seed predation by introduced rodents in Tongan rain forests. Biol Conserv 109:221–225CrossRefGoogle Scholar
  39. McHalick O (1998) Translocation database summary. DOC threatened species occasional publication 14. Department of Conservation, WellingtonGoogle Scholar
  40. Meyer J-Y, Butaud J-F (2008) The impacts of rats on the endangered native flora of French Polynesia (Pacific Islands): drivers of plante extinction or coup de grâce species? Biol Invasions. doi: 10.1007/s10530-008-9407-y Google Scholar
  41. Miskelly CM, Taylor GA (2004) Establishment of a colony of common diving petrels (Pelacanoides urinatrix) by chick transfers and acoustic attraction. Emu 104:205–211CrossRefGoogle Scholar
  42. Mulder CPH, Keall S (2001) Burrowing seabirds and reptiles: impacts on seeds, seedlings and soils in an island forest in New Zealand. Oecologia 127:350–360CrossRefGoogle Scholar
  43. Newman DG (1987) Tuatara. John McIndoe and Department of Conservation, DunedinGoogle Scholar
  44. Nogales M, Medina FM, Quilis V, Gonzalez-Rodriguez M (2001) Ecological and biogeographical implications of yellow-legged gulls (Larus cachinnans Pallas) as seed dispersers of Rubia fruticosa Ait. (Rubiaceae) in the Canary Islands. J Biogeog 28:1137–1145CrossRefGoogle Scholar
  45. Okazaki M, Oshida Y, Malony R, Warham J (1993) Effects of sooty shearwaters Puffinus griseus on surface soils on Motuara Island, New Zealand. J Yamashina Inst Ornithol 25:137–143Google Scholar
  46. Parker PW, Kress SW, Golightly RT, Carter HR, Parsons EB, Schubel SE, Boyce JA, McChewnsy GJ, Wisely SM (2007) Assessment of social attraction techniques used to restore a common murre colony in central California. Waterbirds 30:17–28CrossRefGoogle Scholar
  47. Pascal M, Siorat F, Lorvelect O, Yesou P, Simberloff D (2005) A pleasing consequence of Norway rat eradication: two shrew species recover. Divers Distrib 11:193–198CrossRefGoogle Scholar
  48. 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 147:396–423CrossRefGoogle Scholar
  49. Price ML, Butler LG (1977) Rapid visual estimation of and spectrophotometric determination of tannin content of sorghum grain. J Agric Food Chem 25:1268–1273CrossRefGoogle Scholar
  50. Priddel D, Carlile N, Wheeler R (2006) Establishment of a new breeding colony of Gould’s petrel (Pterodroma leucoptera leucoptera) through the creation of artificial nesting habitat and the translocation of nestlings. Biol Conserv 128:553–563CrossRefGoogle Scholar
  51. Ramsey GW (1978) A review of the effect of rodents on the New Zealand invertebrate fauna. In: Dingwall PR, Atkinson IAE, Hay C (eds) The ecology and control of rodents in New Zealand nature reserves, Department of Lands and Survey Information Series No. 4, pp 89–95Google Scholar
  52. Roberts CM, Duncan RP, Wilson KJ (2007) The effects of burrowing seabirds on forest regeneration, Rangatira Island, Chatham Islands, New Zealand. New Zeal J Ecol 31:208–222Google Scholar
  53. Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18:648–656CrossRefGoogle Scholar
  54. Simberloff D (1990) Reconstructing the ambiguous: can island ecosystems be restored? In: Towns DR, Daugherty CH, Atkinson IAE (eds) Ecological restoration of New Zealand islands. Department of Conservation, Wellington, pp 37–51Google Scholar
  55. Sinclair L, McCartney J, Godfrey J, Pledger S, Wakelin M, Sherley G (2005) How did invertebrates respond to eradication of rats from Kapiti Island, New Zealand? New Zeal J Zool 32:293–315Google Scholar
  56. Smith DG, Shiinoki EK, VanderWerf EA (2006) Recovery of native species following rat eradication on Mokoli’i Island, O’ahu, Hawai’i. Pac Sci 60:299–303CrossRefGoogle Scholar
  57. Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53PubMedCrossRefGoogle Scholar
  58. Towns DR, Daugherty CH (1994) Patterns of range contractions and extinctions in the New Zealand herpetofauna following human colonisation. New Zeal J Zool 21:325–339Google Scholar
  59. Traveset A, Riera N (2005) Disruption of a plant-lizard seed dispersal system and its ecological effects on a threatened endemic plant in the Balearic Islands. Conserv Biol 19:421–431CrossRefGoogle Scholar
  60. Vidal E, Médail F, Tatoni T (2000) Seabirds drive plant species turnover on small Mediterranean Islands at the expense of native taxa. Oecologia 122:427–434CrossRefGoogle Scholar
  61. Wainwright 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 131:63–71CrossRefGoogle Scholar
  62. Wait DA, Aubrey D, Anderson WB (2005) Seabird guano influences on desert islands: soil chemistry and herbaceous species richness and productivity. J Arid Environ 60:681–695CrossRefGoogle Scholar
  63. Ward WT (1961) Soils of Stephens Island. New Zeal J Sci 4:493–505Google Scholar
  64. Wardle DA, Bellingham PJ, Fukami T, Mulder CPH (2007) Promotion of ecosystem carbon sequestration by invasive predators. Biol Lett 3:479–482PubMedCrossRefGoogle Scholar
  65. Whitaker AH (1973) Lizard populations on islands with and without Polynesian rats, Rattus exulans (Peale). Proc New Zeal Ecol Soc 20:121–130Google Scholar
  66. Wolfe KM, Mills HR, Garkaklis MJ, Bencini R (2004) Post-mating survival in a small marsupial is associated with nutrient inputs from seabirds. Ecology 85:1740–1746CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Christa P. H. Mulder
    • 1
  • M. Nicole Grant-Hoffman
    • 1
  • David R. Towns
    • 2
  • Peter J. Bellingham
    • 3
  • David A. Wardle
    • 3
    • 4
  • Melody S. Durrett
    • 1
  • Tadashi Fukami
    • 3
    • 5
  • Karen I. Bonner
    • 3
  1. 1.Institute of Arctic Biology, Department of Biology and WildlifeUniversity of Alaska FairbanksFairbanksUSA
  2. 2.Research and Development GroupDepartment of ConservationAucklandNew Zealand
  3. 3.Manaaki Whenua-Landcare ResearchLincolnNew Zealand
  4. 4.Department of Forest Vegetation EcologySwedish University of Agricultural SciencesUmeåSweden
  5. 5.Department of BiologyStanford UniversityStanfordUSA

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