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Early colonisation population structure of a Norway rat island invasion

  • Invasive Rodents on Islands
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Abstract

Colonists undergo non-equilibrium processes such as founder effects, inbreeding and changing population size which influence the mating system and demography of a population. Understanding these processes in colonising populations informs management and helps prevent further invasions. We sampled and genotyped most individuals of a Norway rat (Rattus norvegicus) reinvasion on Moturemu island (5 ha) in New Zealand. Population size was most likely between 30 and 33 rats. Genetic methods detected a clear bottleneck signal from the founding population. Parentage assignment revealed promiscuous mating dominated by a few individuals with increasing inbreeding, both putatively a result of small island size. Combining ecological and genetic data from a single sample allowed inferences on population structure and functioning. Invading Norway rats rapidly achieve population structure similar to established island populations despite a small number of colonists and associated inbreeding. Overcoming these initial obstacles to population establishment contributes to the global success of invasive rats.

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References

  • Abdelkrim J, Pascal M, Calmet C, Samadi S (2005a) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518

    Article  Google Scholar 

  • Abdelkrim J, Pascal M, Samadi S (2005b) Island colonization and founder effects: the invasion of the Guadeloupe islands by ship rats (Rattus rattus). Mol Ecol 14:2923–2931

    Article  PubMed  CAS  Google Scholar 

  • Allen RB, Duncan RP, Lee WG (2006) Updated perspectives on biological invasions in New Zealand. In: Allen RB, Lee WG (eds) Biological invasions in New Zealand. Springer, Berlin, pp 435–451

    Chapter  Google Scholar 

  • Atkinson IAE (1985) The spread of commensal species of Rattus to oceanic islands and their effects on island avifaunas. In: Moors PJ (ed) Conservation of island birds. International Council for Bird Preservation Technical Publication No. 3, Cambridge, pp 35–81

    Google Scholar 

  • Brigham AJ, Sibley RM (1999) A review of the phenomenon of neophobia. In: Cowan DP, Feare CJ (eds) Advances in vertebrate pest management. Filander Verlag, Furth, pp 67–84

    Google Scholar 

  • Brown KP, Moller H, Innes J, Alterio N (1996) Calibration of tunnel tracking rates to estimate relative abundance of ship rats (Rattus rattus) and mice (Mus musculus) in a New Zealand forest. N Z J Ecol 20:271–275

    Google Scholar 

  • Chakraborty R, Jin L (1993) Determination of relatedness between individuals using DNA fingerprinting. Hum Biol 65:875–895

    PubMed  CAS  Google Scholar 

  • Clout MN, Russell JC (2006) The eradication of introduced mammals from New Zealand islands. In: Koike F, Clout MN, Kawamichi M, De Poorter M, Iwatsuki K (eds) Assessment and control of biological invasion risks. IUCN, Gland, Switzerland and Cambridge U.K. and Shoukadoh Book Sellers, Kyoto, Japan, pp 127–141

    Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Cunningham DM, Moors PJ (1996) Guide to the identification and collection of New Zealand rodents. Department of Conservation, Wellington

    Google Scholar 

  • D’Antonio CM, Dudley TL (1995) Biological invasions as agents of change on islands versus mainlands. In: Vitousek PM, Loope LL, Anderson H (eds) Islands: biological diversity and ecosystem function. Springer, Berlin, pp 103–121

    Google Scholar 

  • Dewsbury DA (1985) Paternal behavior in rodents. Am Zool 25:841–852

    Google Scholar 

  • Efford MG, Fitzgerald BM, Karl BJ, Berben PH (2006) Population dynamics of the ship rat Rattus rattus L. in the Orongorongo Valley, New Zealand. N Z J Zool 33:273–297

    Google Scholar 

  • Estoup A, Wilson IJ, Sullivan C, Cornuet JM, Moritz C (2001) Inferring population history from microsatellite and enzyme data in serially introduced cane toads, (Bufo marinus). Genetics 159:1671–1687

    PubMed  CAS  Google Scholar 

  • Excoffier L, Heckel G (2006) Computer programs for population genetics data analysis: a survival guide. Nat Rev Genet 7:745–758

    Article  PubMed  CAS  Google Scholar 

  • Fukami T, Wardle DA, Bellingham PJ et al (2006) Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 9:1299–1307

    Article  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Glass GE, Korch GW, Childs JE (1988) Seasonal and habitat differences in growth rates of wild Rattus norvegicus. J Mammal 69:587–592

    Article  Google Scholar 

  • Gould WR, Pollock KH (1997) Catch-effort maximum likelihood estimation of important population parameters. Can J Fish Aquat Sci 54:890–897

    Article  Google Scholar 

  • Heiberg A-C, Leirs H, Siegismund HR (2006) Reproductive success of bromadiolone-resistant rats in the absence of anticoagulant pressure. Pest Manage Sci 62:862–871

    Article  CAS  Google Scholar 

  • Herborg L-M, Weetman D, Oosterhout CV, Hänfling B (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader, the Chinese mitten crab, Eriocheir sinensis. Mol Ecol 16:231–242

    Article  PubMed  CAS  Google Scholar 

  • Hirst D (1994) An improved removal method for estimating animal abundance. Biometrics 50:501–505

    Article  PubMed  CAS  Google Scholar 

  • Howald G, Donlan CJ, Galván JP et al (2007) Invasive rodent eradication on islands. Conserv Biol 21:1258–1268

    Article  PubMed  Google Scholar 

  • Imber M, Harrison M, Harrison J (2000) Interactions between petrels, rats and rabbits on Whale Island, and effects of rat and rabbit eradication. N Z J Ecol 24:153–160

    Google Scholar 

  • Innes JG (2005) Norway rat. In: King CM (ed) The handbook of New Zealand mammals. Oxford University Press, Melbourne, pp 187–203

    Google Scholar 

  • Jacob HJ, Brown DM, Bunker RK et al (1995) A genetic linkage map of the laboratory rat, Rattus norvegicus. Nat Genet 9:63–69

    Article  PubMed  CAS  Google Scholar 

  • Jamieson IG, Tracy LN, Fletcher D, Armstrong DP (2007) Moderate inbreeding depression in a reintroduced population of North Island robins? Anim Conserv 10:95–102

    Article  Google Scholar 

  • Jones HP, Tershy BR, Zavaleta ES et al (2008) Severity of the effects of invasive rats on seabirds: a global review. Conserv Biol 22:16–26

    Article  PubMed  Google Scholar 

  • Kaeuffer R, Coltman DW, Chapuis J-L, Pontier D, Réale D (2007) Unexpected heterozygosity in an island mouflon population founded by a single pair of individuals. Proc R Soc Lond Ser B 274:527–533

    Article  CAS  Google Scholar 

  • Liu L, Yip PSF, Watson RK (2003) Removal process estimation of population size for a population with a known sex ratio. Environ Ecol Stat 10:281–292

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  PubMed  CAS  Google Scholar 

  • Macdonald DW, Mathews F, Berdoy M (1999) The behaviour and ecology of Rattus norvegicus: from opportunism to kamikaze tendencies. In: Singleton GR, Hinds LA, Leirs H, Zhang Z (eds) Ecologically-based rodent management. ACIAR Monograph No. 59, Canberra, pp 49–80

    Google Scholar 

  • Manly BFJ (1985) The statistics of natural selection. Chapman and Hall, London

    Google Scholar 

  • Mäntyniemi S, Romakkaniemi A, Arjas E (2005) Bayesian removal estimation of a population size under unequal catchability. Can J Fish Aquat Sci 62:291–300

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Moller H, Tilley JAV (1986) Rodents and their predators in the eastern Bay of Islands. N Z J Zool 13:563–572

    Google Scholar 

  • Moors PJ (1985) Norway rats (Rattus norvegicus) on the Noises and Motukawao Islands, Hauraki Gulf, New Zealand. N Z J Ecol 8:37–54

    Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  PubMed  CAS  Google Scholar 

  • Parkes J (2006) Eradication of vertebrate pests: are there any general lessons? In: Feare CJ, Cowan DP (eds) Advances in vertebrate pest management IV. Filander Verlag, Furth, pp 91–110

    Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reduction in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact test and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Robertson BC, Gemmell NJ (2004) Defining eradication units: introduced brown rats Rattus norvegicus on South Georgia, Southern Ocean. J Appl Ecol 41:1042–1048

    Article  Google Scholar 

  • Routledge RD (1985) The removal method for estimating natural populations: incorporating auxiliary information. Biometrics 45:111–121

    Article  Google Scholar 

  • Russell JC, Clout MN (2005) Rodent incursions on New Zealand islands. In: Parkes J, Statham M, Edwards G (eds) Proceedings of the 13th Australasian vertebrate pest conference. Landcare Research, Lincoln, pp 324–330

  • Russell JC, Fewster RM (2009) Evaluation of the linkage disequilibrium method for estimating effective population size. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Environmental and Ecological Statistics Series, vol 3. Springer, Berlin, pp 291–320

  • Russell JC, Towns DR, Anderson SH, Clout MN (2005) Intercepting the first rat ashore. Nature 437:1107

    Article  PubMed  CAS  Google Scholar 

  • Russell JC, Beaven BM, MacKay JWB, Towns DR, Clout MN (2008) Testing island biosecurity systems for invasive rats. Wildl Res 35:215–221

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Seber GAF (1982) The estimation of animal abundance and related parameters. The Blackburn Press, Caldwell

    Google Scholar 

  • Slate J, Marshall TC, Pemberton JM (2000) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9:801–808

    Article  PubMed  CAS  Google Scholar 

  • Solomon NG, Keane B (2007) Reproductive strategies in female rodents. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 42–56

    Google Scholar 

  • Stockley P (2003) Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc R Soc Lond Ser B 270:271–278

    Article  CAS  Google Scholar 

  • Taylor RH, Thomas BW (1993) Rats eradicated from rugged Breaksea Island (170 ha), Fiordland, New Zealand. Biol Conserv 65:191–198

    Article  Google Scholar 

  • Thomas MD, Brown JA, Henderson RJ (1999) Feasibility of using wax blocks to measure rat and possum abundance in native forest. Proc N Z Plant Prot Conf 52:125–129

    Google Scholar 

  • Thorsen M, Shorten R, Lucking R, Lucking V (2000) Norway rats (Rattus norvegicus) on Frégate Island, Seychelles: the invasion; subsequent eradication attempts and implications for the island’s fauna. Biol Conserv 96:133–138

    Article  Google Scholar 

  • Thulin C-G, Simberloff D, Barun A, McCracken G, Pascal M, Islam MA (2006) Genetic divergence in the small Indian mongoose (Herpestes auropunctatus), a widely distributed invasive species. Mol Ecol 15:3947–3956

    Article  PubMed  CAS  Google Scholar 

  • Towns DR, Broome KG (2003) From small Maria to massive Campbell: forty years of rat eradications from New Zealand islands. N Z J Zool 30:377–398

    Google Scholar 

  • Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8:863–891

    Article  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16

    Google Scholar 

  • Waterman J (2007) Male mating strategies in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 27–41

    Google Scholar 

  • Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associates, Sunderland

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

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Acknowledgments

This research was funded by the Department of Conservation and performed under the appropriate Department of Conservation research and University of Auckland animal ethics permits. James Russell was supported by a Top Achiever Doctoral Scholarship and an Edward and Isabel Kidson Scholarship. Rachel Fewster was supported by a Marsden grant from the Royal Society of New Zealand. Genetics analysis was made possible by an International Sciences and Technology (ISAT) Linkages grant to James Russell from the Royal Society of New Zealand and support from the Muséum National d’Histoire Naturelle, Paris. The authors would like to thank Holly Jones and Steven Miller for assistance in the field, Dave Towns and Peter Crossley for field transportation, the Department of Conservation Warkworth Area Office and in particular Thelma Wilson for discussion and background documentation and Ngati Whatua. Shirley Pledger assisted with catch-effort modelling, and Paul Murrell with graphics. Scott Baker, Karen Nutt, Dave Towns, Mark Hauber, Charlie Daugherty and two anonymous referees provided useful feedback on the manuscript. Thanks to Don Drake and Terry Hunt for inviting this paper into the Proceedings of the Rats, Humans and Islands conference.

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Russell, J.C., Abdelkrim, J. & Fewster, R.M. Early colonisation population structure of a Norway rat island invasion. Biol Invasions 11, 1557–1567 (2009). https://doi.org/10.1007/s10530-008-9406-z

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