Oecologia

, Volume 163, Issue 2, pp 449–460 | Cite as

Invasive rats alter woody seedling composition on seabird-dominated islands in New Zealand

  • Madeline N. Grant-Hoffman
  • Christa P. Mulder
  • Peter J. Bellingham
Community ecology - Original Paper

Abstract

Invasive rats (Rattus rattus, R. norvegicus, R. exulans) have large impacts on island habitats through both direct and indirect effects on plants. Rats affect vegetation by extirpating burrowing seabirds through consumption of eggs, chicks, and adults. These seabirds serve as ecosystem engineers, affecting plant communities by burying and trampling seeds and seedlings, and by altering microclimate. Rats also directly affect plant communities by consuming seeds and seedlings. We studied the direct and indirect impacts of rats on the seedlings of woody plants on 21 islands in northern New Zealand. We compared seedling densities and richness on islands which differed in status with respect to rats: nine islands where rats never invaded, seven islands where rats were present at the time of our study, and five islands where rats were either eradicated or where populations were likely to be small as a result of repeated eradications and re-invasions. In addition, we compared plots from a subset of the 21 islands with different burrow densities to examine the effects of burrowing seabirds on plants while controlling for other factors that differ between islands. We categorized plant communities by species composition and seedling density in a cluster analysis. We found that burrow densities explained more variation in seedling communities than rat status. In areas with high seabird burrow density seedling densities were low, especially for the smallest seedlings. Species richness and diversity of seedlings, but not seedling density, were most influenced by changes in microclimate induced by seabirds. Islands where rats had been eradicated or that had low rat populations had the lowest diversity and richness of seedlings (and adults), but the highest seedling density. Seedling communities on these islands were dominated by Pseudopanax lessonii and Coprosma macrocarpa. This indicates lasting effects of rats that may prevent islands from returning to pre-invasion states.

Keywords

Rattus rattus Rattus norvegicus Ecosystem engineer Seedling community Predator eradication 

Supplementary material

442_2009_1523_MOESM1_ESM.doc (46 kb)
(Doc 47 kb)

References

  1. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second International Symposium on Information Theory. Akademiai Kiado, Budapest, pp 267–281Google Scholar
  2. Allen RB, Lee WG, Rance BD (1994) Regeneration in indigenous forest after eradication of Norway rats, Breaksea Island, New Zealand. NZ J Bot 32:429–439Google Scholar
  3. Anderberg MR (1973) Cluster analysis for applications. Academic Press, New YorkGoogle Scholar
  4. Anderson WB, Polis GA (1999) Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia 118:324–332CrossRefGoogle Scholar
  5. Atkinson IAE (1985) The spread of commensal species of Rattus to oceanic islands and their effects on island avifaunas. ICBP Tech Publ 3Google Scholar
  6. Atkinson IAE (2004) Successional processes induced by fires on the northern offshore islands of New Zealand. NZ J Ecol 28:181–193Google Scholar
  7. Atkinson IAE (2006) Introduced mammals in a new environment. In: Allen RB, Lee WG (eds) Biological invasions in New Zealand. Springer, Berlin, pp 49–66CrossRefGoogle Scholar
  8. Bancroft WJ, Garkaklis MJ, Roberts JD (2005) Burrowing in seabird colonies: a soil-forming process in island ecosystems. Pedobiologia 49:149–165CrossRefGoogle Scholar
  9. Bellingham PJ, Sparrow AD (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89:409–415CrossRefGoogle Scholar
  10. Bellingham PJ, Towns DR, Cameron EK, Davis JJ, Wardle DA, Wilmshurst JM, Mulder CPH (2010) New Zealand island restoration: seabirds, predators, and the importance of history. NZ J Ecol 34:115–135Google Scholar
  11. Blakemore LC, Gibbs HS (1968) Effects of gannets on soil at Cape Kidnappers, Hawke’s Bay. NZ J Sci 11:54–62Google Scholar
  12. Burger AE, Lindeboom HJ, Williams AJ (1978) The mineral and energy contributions of guano of selected species of birds to the Marion Island terrestrial ecosystem. S Afr J Antarct 8:59–70Google Scholar
  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  14. Cameron EK (1990) Flora and vegetation of Middle Island, Mercury Islands Group, eastern Coromandel, northern New Zealand. J R Soc NZ 20:273–285Google Scholar
  15. Cameron EK, de Lange PJ, McCallum J, Taylor GA, Bellingham PJ (2007) Vascular flora and some fauna for a chain of six Hauraki Gulf islands east and southeast of Waiheke Island. Auckl Bot Soc J 62:136–156Google Scholar
  16. Campbell DJ (1978) The effects of rats on vegetation. 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 9–120Google Scholar
  17. Campbell DJ (2002) Changes in numbers of woody plant seedlings on Kapiti Island after rat eradication. Sci Conserv 193:5–26Google Scholar
  18. 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 NZ 29:265–291Google Scholar
  19. 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
  20. Campbell DJ, Moller H, Ramsay GW, Watt JC (1984) Observations on foods of kiore (Rattus exulans) found in husking stations on northern offshore islands of New Zealand. NZ J Ecol 7:131–138Google Scholar
  21. Carter J (2002) Nest-site selection and breeding success of wedge-tailed shearwaters Puffinus pacificus at Heron Island. Aust Geogr Stud 35:153–167CrossRefGoogle Scholar
  22. Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383CrossRefPubMedGoogle Scholar
  23. Court DJ, Hardacre AK, Lynch PA (1973) The vegetation of the Aldermen Islands: a reappraisal. Tane 19:41–67Google Scholar
  24. Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV (2005) Introduced predators transform subartic islands from grassland to tundra. Science 307:1959–1961CrossRefPubMedGoogle Scholar
  25. de Lange WP, de Lange PJ, Moon VG (2006) Boulder transport by waterspouts: an example from Aorangi Island, New Zealand. Marine Geol 230:115–125CrossRefGoogle Scholar
  26. Drake DR, Hunt TL (2009) Invasive rodents on islands: integrating historical and contemporary ecology. Biol Invasions 11:1671–1688CrossRefGoogle Scholar
  27. Drever MC, Harestad AA (1998) Diets of Norway rats, Rattus norvegicus, on Langara Island, Queen Charlotte Islands, British Columbia: implications for conservation of breeding seabirds. Can Field Nat 112:676–683Google Scholar
  28. 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
  29. Fountain DW, Outred HA (1991) Germination requirements of New Zealand native plants: a review. NZ J Bot 29:311–316Google Scholar
  30. 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 9:1299–1307CrossRefPubMedGoogle Scholar
  31. 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 53–65Google Scholar
  32. Gaze P (2000) The response of a colony of sooty shearwater (Puffinus griseus) and flesh-footed shearwater (P. carneipes) to the cessation of harvesting and the eradication of Norway rats (Rattus norvegicus). NZ J Zool 27:381–393Google Scholar
  33. Gillham ME (1960) Destruction of indigenous heath vegetation in Victorian sea-bird colonies. Aust J Bot 8:277–317CrossRefGoogle Scholar
  34. Gillham ME (1961) Some interactions of plants, rabbits and seabirds on South African islands. J Ecol 49:275–294Google Scholar
  35. Goldberg DE, Scheiner SM (2001) ANOVA and ANCOVA: field competition experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, New York, pp 77–98Google Scholar
  36. Gotelli NJ, Entsminger GL (2006) EcoSim: Null models software for ecology. Version 7. Acquired Intelligence, Kesey-Bear, Jericho, Vt. http://garyentsminger.com/ecosim.htm
  37. Grant-Hoffman MN, Barboza PS (2010) Herbivory in invasive rats: Criteria for food selection. Biol Inv. doi:10.1007/s10530-009-9503-7 Google Scholar
  38. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910CrossRefGoogle Scholar
  39. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control and competition. Am Nat 94:421–425CrossRefGoogle Scholar
  40. Hawke DJ, Newman J (2004) Inventories and elemental accumulation in peat soils of forested seabird breeding islands, southern New Zealand. Aust J Soil Res 42:45–48CrossRefGoogle Scholar
  41. Hilhorst HWM, Karssen CM (2000) Effect of chemical environment on seed germination. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI Publishing, Wallingford, pp 293–310CrossRefGoogle Scholar
  42. Holdaway RN (1999) A spatio-temporal model for the invasion of the New Zealand archipelago by the Pacific rat Rattus exulans. J R Soc NZ 25:91–105Google Scholar
  43. Howald G, Donlan 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 21:1258–1268CrossRefPubMedGoogle Scholar
  44. 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. Conserv Biol 22:16–26CrossRefPubMedGoogle Scholar
  45. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, PrincetonGoogle Scholar
  46. Maesako Y (1999) Impacts of streaked shearwater (Calonectris leucomelas) on tree seedling regeneration in a warm-temperate evergreen forest on Kanmurijima Island, Japan. Plant Ecol 145:183–190CrossRefGoogle Scholar
  47. Major HL, Jones IL, Charette MR, Diamond AW (2007) Variations in the diet of introduced Norway rats (Rattus norvegicus) inferred using stable isotope analysis. J Zool 271:463–468CrossRefGoogle Scholar
  48. McLaren RG, Cameron KC (1990) Soil science. Oxford University Press, OxfordGoogle Scholar
  49. 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
  50. Mizutani H, Wada W (1988) Nitrogen and carbon isotope ratios in seabird rookeries and their ecological impacts. Ecology 69:340–349CrossRefGoogle Scholar
  51. Mulder CPH, Keall SN (2001) Burrowing seabirds and reptiles: impacts on seeds, seedlings and soils in an island forest in New Zealand. Oecologia 127:350–360CrossRefGoogle Scholar
  52. 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 11:1671–1688CrossRefGoogle Scholar
  53. 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
  54. Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265CrossRefGoogle Scholar
  55. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75CrossRefGoogle Scholar
  56. Poole AL, Adams NM (1964) Trees and shrubs of New Zealand. Owen. Government Printer, WellingtonGoogle Scholar
  57. Priddel D, Carlile N, Wheeler R (2006) Establishment of a new breeding colony of Gould’s petrel (Pterodroma leucoptera) through the creation of artificial nesting habitat and the translocation of nestlings. Biol Conserv 128:553–563CrossRefGoogle Scholar
  58. SAS Institute (2003) The SAS system for Windows V9.1. SAS Institute, CaryGoogle Scholar
  59. Scheiner SM (2001) MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, Oxford, pp 99–115Google Scholar
  60. Schmitz OJ, Hamback PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153CrossRefPubMedGoogle Scholar
  61. Stephens PA, Buskirk SW, Hayward GD, Martinez Del Rio C (2005) Information theory and hypothesis testing: a call for pluralism. J Appl Ecol 42:4–12CrossRefGoogle Scholar
  62. Terborgh J, Lopez L, Nunez VP, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Alder GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1925CrossRefPubMedGoogle Scholar
  63. Thorsen M, Shorten R, Lucking R, Lucking V (2000) Norway rats (Rattus norvegicus) on Fregate Island, Seychelles: the invasion; subsequent eradication attempts and implications for the island’s fauna. Biol Conserv 96:133–138CrossRefGoogle Scholar
  64. Towns DR, Broome KG (2003) From small Maria to massive Campbell: forty years of rat eradications from New Zealand islands. NZ J Zool 30:377–398Google Scholar
  65. Towns DR, Daugherty CH (1994) Patterns of range contractions and extinctions in the New Zealand herpatofauna following human colonization. NZ J Zool 21:325–339Google Scholar
  66. Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8:863–891CrossRefGoogle Scholar
  67. 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 118:420–430CrossRefGoogle Scholar
  68. Wainright SC, Haney JC, Kerr C, Golovkin AN, Fling 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
  69. Ward WT (1961) Soils of Stephens Island. NZ J Sci 4:493–505Google Scholar
  70. Wardle DA, Bellingham PJ, Fukami T, Mulder CPH (2007) Promotion of ecosystem carbon sequestration by invasive predators. Biol Lett 3:479–482CrossRefPubMedGoogle Scholar
  71. Wardle DA, Bellingham PJ, Bonner KI, Mulder CPH (2009) Indirect effects of invasive predators on plant litter quality, decomposition, and nutrient resorption on seabird-dominated islands. Ecology 90:452–464CrossRefPubMedGoogle Scholar
  72. Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, LondonGoogle Scholar
  73. Wilson DJ, Lee WG, Webster RA, Allen RB (2003) Effects of possums and rats on seedling establishment at two forest sites in New Zealand. NZ J Ecol 27:147–155Google Scholar
  74. Worthy TH, Holdaway RN (2002) Oceanic birds in the terrestrial environment. In: The lost world of the Moa. Canterbury University Press, Christchurch, pp 440–501Google Scholar
  75. Worthy TH, Tennyson AJD, Archer M, Musser AN, Hand SJ, Jones C, Douglas BJ, McNamara JA, Beck RMD (2006) Miocene mammal reveals a Mesozoic ghost lineage on insular New Zealand, southwest Pacific. Proc Natl Acad Sci USA 103:10419–19423CrossRefGoogle Scholar
  76. Yodzis P (1988) The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology 69:508–515CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Madeline N. Grant-Hoffman
    • 1
    • 4
  • Christa P. Mulder
    • 1
    • 2
  • Peter J. Bellingham
    • 3
  1. 1.Department of Biology and WildlifeUniversity of Alaska FairbanksFairbanksUSA
  2. 2.Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA
  3. 3.Landcare ResearchLincolnNew Zealand
  4. 4.National Landscape Conservation System, Grand Junction Field OfficeBureau of Land Management ColoradoGrand JunctionUSA

Personalised recommendations