Biological Invasions

, 13:2391 | Cite as

Reinvasion by ship rats (Rattus rattus) of forest fragments after eradication

  • Carolyn M. KingEmail author
  • John G. Innes
  • Dianne Gleeson
  • Neil Fitzgerald
  • Tom Winstanley
  • Barry O’Brien
  • Lucy Bridgman
  • Neil Cox
Original Paper


Reinvasions provide prime examples of source-sink population dynamics, and are a major reason for failure of eradications of invasive rats from protected areas. Yet little is known about the origins and population structure of the replacement population compared with the original one. We eradicated eight populations of ship rats from separate podocarp-broadleaved forest fragments surrounded by open grassland (averaging 5.3 ha, scattered across 20,000 ha) in rural landscapes of Waikato, New Zealand, and monitored the- re-establishment of new populations. Rats were kill-trapped to extinction during January to April 2008, and then again after reinvasion in April–May (total n = 517). Rats carrying Rhodamine B dye (n = 94), available only in baits placed 1–2 months in advance in adjacent source areas located 170–380 m (average 228 m edge to edge) away, appeared in 7 of the 8 fragments from the first day of the first eradication. The distribution of age groups, genders and proportions of reproductively mature adults (more immature juvenile males and fewer fully mature old females) was different among marked rats compared with all other rats (P = 0.001, n = 509); in all rats caught on days 7+ of the first eradication compared with on days 1–6 (P = 0.000); and in the total sample collected in fragments by trapping to and after local extinction compared with in brief, fixed-schedule sampling of populations in continuous forests (P = 0.000). Genotyping of 493 carcases found no significant population-level differentiation among the 8 fragments, confirming that the rats in all fragments belonged to a single dynamic metapopulation. Marked rats of both genders travelled up to 600 m in a few days. Conservation of forest fragments is compromised by the problem that ship rats cannot be prevented from rapidly reinvading any cleared area after eradication.


Invasive predators Reinvasion Roof rat Black rat Forest fragment Genetic differentiation Eradication units 



We gratefully acknowledge the landowners and managers who generously gave us free access to their forest fragments: Lyndon Bergerson, Shane Blair, Paul and Jo Bodle, Mr R.A. Boyte, Bill Boyte, Des McAllister, Allen Marr, Greg and Jackie Nicholls, Brett and Narelle Pollock, Deborah and John Stretton. Chris Floyd helped locate study sites, and Penny Fisher gave valuable advice about Rhodamine B marking. Scott Bartlam, Sam Cave, Toni Cornes, and particularly Stacey Foster and Jordan Edgar helped with the substantial fieldwork required for this project, including daily trap-clearing that lasted several months. The manuscript was greatly improved by the perceptive comments of two anonymous referees. The research was funded by the Foundation for Research, Science and Technology under UOW X0609 and the 2010 Strategic Investment Fund of Waikato University. Approval for the Rhodamine B bait-marking work was granted under Waikato University Animal Ethics Protocol No. 707.


  1. Abdelkrim J, Pascal M, Calmet C, Samadi S (2005) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19(5):1509–1518. doi: 10.1111/j.1523-1739.2005.00206.x ISSN0888-8892CrossRefGoogle Scholar
  2. Abdelkrim J, Pascal M, Samadi S (2007) Establishing causes of eradication failure based on genetics: case study of ship rat eradication in Ste. Anne archipelago. Conserv Biol 21:719–730PubMedCrossRefGoogle Scholar
  3. Abdelkrim J, Pascal M, Samadi S (2009) Genetic structure and functioning of alien ship rat populations from a Corsican micro-insular complex. Biol Invasions 11(3):473–482CrossRefGoogle Scholar
  4. Abdelkrim J, Byrom AE, Gemmell NJ (2010) Fine-scale genetic structure of mainland invasive Rattus rattus populations: implications for restoration of forested conservation areas in New Zealand. Conserv Genet 11:1953–1964CrossRefGoogle Scholar
  5. Armstrong D, Raeburn E, Lewis R, Ravine D (2006a) Estimating the viability of a reintroduced New Zealand robin population as a function of predator control. J Wildl Manage 70:1020–1027CrossRefGoogle Scholar
  6. Armstrong D, Raeburn E, Lewis R, Ravine D (2006b) Modeling vital rates of a reintroduced New Zealand robin population as a function of predator control. J Wildl Manage 70:1028–1036CrossRefGoogle Scholar
  7. Atkinson IAE (1973) Spread of the ship rat (Rattus r. rattus L.) in New Zealand. J Roy Soc NZ 3(3):457–472Google Scholar
  8. Bentley JM (2008) Role of movement, interremnant dispersal and edge effects in determining sensitivity to habitat fragmentation in two forest-dependant rodents. Austral Ecol 33:184–196CrossRefGoogle Scholar
  9. Bowne DR, Bowers MA (2004) Interpatch movements in spatially structured populations: a literature review. Landscape Ecol 19:1–20CrossRefGoogle Scholar
  10. Brooke MD, Hilton GM, Martins TLF (2007) Prioritizing the world’s islands for vertebrate-eradication programmes. Anim Conserv 10(3):380–390. doi: 10.1111/j.1469-1795.2007.00123.x CrossRefGoogle Scholar
  11. Brown KP, Moller H, Innes J, Jansen P (1998) Identifying predators at nests of small birds in a New Zealand forest. Ibis 140(2):274–279CrossRefGoogle Scholar
  12. Burns BR, Floyd CG, Smale MC, Arnold GC (2010) Effects of forest fragment management on vegetation condition and maintenance of canopy composition in a New Zealand pastoral landscape. Austral Ecol. doi: 10.1111/j.1442-9993.2010.02130.x
  13. Calhoun JB (1963) The ecology and sociobiology of the Norway rat. United States Department of Health, Education and Welfare, Public Health Service Publication 1008, Bethesda, MarylandGoogle Scholar
  14. Clarkson BD, Merrett M, Downs T (2002) Botany of the Waikato. Waikato Botanical Society, HamiltonGoogle Scholar
  15. Connolly TA, Day TD, King CM (2009) Estimating the potential for re-invasion by mammalian pests through pest-exclusion fencing. Wildl Res 36:410–421CrossRefGoogle Scholar
  16. Department of Conservation and Ministry for the Environment (2000) The New Zealand Biodiversity Strategy. Department of Conservation and Ministry for the Environment, WellingtonGoogle Scholar
  17. Didham RK, Barker GM, Costall JA, Denmead L, Floyd C, Watts CH (2009) The interactive effects of livestock exclusion and mammalian pest control on the restoration of invertebrate communities in small forest fragments. N Z J Zool 36:135–163Google Scholar
  18. Dilks P, Willans M, Pryde M, Fraser I (2003) Large scale stoat control to protect mohua (Mohoua ochrocephala) and kaka (Nestor meridionalis) in the Eglinton Valley, Fiordland, New Zealand. N Z J Ecol 27(1):1–9Google Scholar
  19. Dodd M, Barker G, Burns B, Didham R, Innes J, King C, Smale M, Watts C (2011) The resilience of New Zealand indigenous forest fragments to impacts of livestock and pest mammals. N Z J Ecol 35:83–95Google Scholar
  20. Fisher P (1999) Review of using Rhodamine B as a marker for wildlife studies. Wildlife Soc B 27:318–329Google Scholar
  21. Foster SP, King CM, Patty B, Miller SD (2011) Tree-climbing capabilities of Norway and ship rats. N Z J Zool 38. doi: 10.1080/03014223.2011.599400
  22. Gardner-Santana LC, Norris DE, Fornadel CM, Hinson ER, Klein SL, Glass GE (2009) Commensal ecology, urban landscapes, and their influence on the genetic characteristics of city-dwelling Norway rats (Rattus norvegicus). Mol Ecol 18:2766–2778PubMedCrossRefGoogle Scholar
  23. Gibbs G (2009) The end of an 80-million year experiment: a review of evidence describing the impact of introduced rodents on New Zealand’s ‘mammal-free’ invertebrate fauna. Biol Invasions 11(7):1587–1593. doi: 10.1007/s10530-008-9408-x CrossRefGoogle Scholar
  24. Gleeson D, Byrom AE, Howitt RLJ (2010) Non-invasive methods for genotyping of stoats (Mustela erminea) in New Zealand: potential for field applications. N Z J Ecol 34:356–359Google Scholar
  25. Goudet J (1995) Fstat version 12: a computer program to calculate Fstatistics. J Hered 86(6):485–486Google Scholar
  26. Green W, Clarkson BD (2006) Turning the tide? A review of the first five years of the New Zealand Biodiversity Strategy: the synthesis report. Department of Conservation WellingtonGoogle Scholar
  27. Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A, Harrison S, Holland M, Lambrinos J, Malvadkar U, Melbourne BA, Moore K, Taylor C, Thomson D (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101CrossRefGoogle Scholar
  28. Hooker S, Innes J (1995) Ranging behaviour of forest-dwelling ship rats, Rattus rattus, and effects of poisoning with brodifacoum. N Z J Zool 22:291–304Google Scholar
  29. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedCrossRefGoogle Scholar
  30. Innes JG (2005) Ship rat. In: King CM (ed) The handbook of New Zealand mammals, 2nd edn. Oxford University Press, Melbourne, pp 187–203Google Scholar
  31. Innes J, Warburton B, Williams D, Speed H, Bradfield P (1995) Large-scale poisoning of ship rats (Rattus rattus) in indigenous forests of the North Island, New Zealand. N Z J Ecol 19(1):5–17Google Scholar
  32. Innes JG, Hay R, Flux I, Bradfield P, Speed H, Jansen P (1999) Successful recovery of North Island kokako Callaeas cinerea wilsoni populations, by adaptive management. Biol Conserv 87(2):201–214CrossRefGoogle Scholar
  33. Innes JG, King CM, Flux M, Kimberley MO (2001) Population biology of the ship rat and Norway rat in Pureora Forest Park 1982–1987. N Z J Zool 28(1):57–78Google Scholar
  34. Innes J, Kelly D, Overton J, Gillies C (2010a) Predation and other factors currently limiting New Zealand forest birds. N Z J Ecol 34(1):86–114Google Scholar
  35. Innes J, King CM, Bridgman L, Fitzgerald N, Arnold GC, Cox N (2010b) Effect of grazing on ship rat density in forest fragments of lowland Waikato, New Zealand. N Z J Ecol 34(2):227–232Google Scholar
  36. Jacob HJ, Brown DM, Bunker RK, Daly MJ, Dzau VJ, Goodman A, Koike G, Kren V, Kurtz T, Lernmark A et al (1995) A genetic linkage map of the laboratory rat, Rattus norvegicus. Nature Genet 9:63–69PubMedCrossRefGoogle Scholar
  37. Krebs CJ, Lambin X, Wolff JO (2007) Social behaviour and self-regulation in murid rodents. In: Wolff JO, Sherman PW (eds) Rodent species: an ecological and evolutionary perspective. University of Chicago Press, London, pp 173–181Google Scholar
  38. MacQueen PE, Nicholls JA, Hazlitt SL, Goldizen AW (2008) Gene flow among native bush rat, Rattus fuscipes (Rodentia: Muridae), populations in the fragmented subtropical forests of south-east Queensland. Austral Ecol 33:585–593CrossRefGoogle Scholar
  39. Manly BF (1985) The statistics of natural selection on animal populations. Chapman and Hall, New YorkGoogle Scholar
  40. Mills LS, Citta JJ, Lair KP, Schwartz MK, Tallmon DA (2000) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol Appl 10:283–294CrossRefGoogle Scholar
  41. Oosterhout C, Hutchinson W, Willds D, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  42. Pascal M, Brithmer R, Lorvelec O, Venumiere N (2004) Consequences of the Ship Rat (Rattus rattus) recent invasion on the breeding avifauna of Sainte-Anne Islets Natural Reserve (Martinique, French West Indies), established after an eradication attempt. Revue D Ecologie-La Terre Et La Vie 59(1–2):309–318Google Scholar
  43. Peakall R, Lindenmayer D (2006) Genetic insights into population recovery following experimental perturbation in a fragmented landscape. Biol Conserv 132:520–532CrossRefGoogle Scholar
  44. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  45. Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721CrossRefGoogle Scholar
  46. Quy RJ (2003) Adapting baiting tactics to match the foraging behaviour of Norway rats: a balance between efficacy and safety. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM (eds) Rats, mice and people: rodent biology and management, vol Monographs 96. ACIAR, Canberra, pp 451–456Google Scholar
  47. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  48. Russell JC, Abdelkrim J, Fewster RM (2009a) Early colonisation population structure of a Norway rat island invasion. Biol Invasions 11(7):1557–1567CrossRefGoogle Scholar
  49. Russell JC, Mackay JWB, Abdelkrim J (2009b) Insular pest control within a metapopulation context. Biol Conserv 142(7):1404–1410. doi: 10.1016/j.biocon.2009.01.032 CrossRefGoogle Scholar
  50. Russell JC, Miller SD, Harper GA, MacInnes HE, Wylie MJ, Fewster RM (2010) Survivors or reinvaders? Using genetic assignment to identify invasive pests following eradication. Biol Invasions 12(6):1747–1757CrossRefGoogle Scholar
  51. Stokes VL, Banks PB, Pech RP, Spratt DM (2009) Competition in an invaded rodent community reveals black rats as a threat to native bush rats in littoral rainforest of south-eastern Australia. J Appl Ecol 46:1239–1247CrossRefGoogle Scholar
  52. Towns DR (2009) Eradications as reverse invasions: lessons from Pacific rat (Rattus exulans) removals on New Zealand islands. Biol Invasions 11:1719–1733CrossRefGoogle Scholar
  53. Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8(4):863–891CrossRefGoogle Scholar
  54. Walker S, Price R, Rutledge D, Stephens RTT, Lee WG (2006) Recent loss of indigenous cover in New Zealand. N Z J Ecol 30(2):169–177Google Scholar
  55. Watkins AF, McWhirter JL, King CM (2010) Variable detectability in long-term population surveys of small mammals. Eur J Wildl Manage 56(3):261–274CrossRefGoogle Scholar
  56. Watling JI, Donnelly MA (2006) Fragments as Islands: a synthesis of faunal responses to habitat patchiness. Conserv Biol 20(4):1016–1025PubMedCrossRefGoogle Scholar
  57. With KA (2002) The landscape ecology of invasive spread. Conserv Biol 16(5):1192–1203CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Carolyn M. King
    • 1
    Email author
  • John G. Innes
    • 2
  • Dianne Gleeson
    • 3
  • Neil Fitzgerald
    • 2
  • Tom Winstanley
    • 3
  • Barry O’Brien
    • 1
  • Lucy Bridgman
    • 1
    • 2
  • Neil Cox
    • 4
  1. 1.Department of Biological SciencesUniversity of WaikatoHamiltonNew Zealand
  2. 2.Landcare ResearchHamiltonNew Zealand
  3. 3.Ecological Genetics LaboratoryLandcare ResearchAucklandNew Zealand
  4. 4.Invermay Statistics Group, AgResearchInvermay Research CentreMosgielNew Zealand

Personalised recommendations