Abstract
The ship rat or black rat (Rattus rattus) is one of the most widespread invasive rodent species on earth, and is a known cause of extinction of several endemic species in invaded ecosystems. While some information is available for insular populations, very little is known about the genetic population structure of this species on mainland areas. In this study (the first to characterize genetic population structure of invasive R. rattus on the mainland), we focused on the population structure of rats located in Puketi Forest Conservation Reserve, Northland, New Zealand, to help conservation managers optimize control programs. We used eight microsatellite markers and classical population genetics tools (F st, clustering methods) as well as individual-based descriptive methods using GPS coordinates for each sample (Genetic Landscape Shape, Bandwidth Mapping) in order to determine whether there was any undetected genetic structure over the 5-km2 area. Very little genetic structure was detected. Nevertheless, a weak but significant isolation-by-distance pattern was inferred. No isolation with external sites (encompassing an area up to 20 km2) was found, suggesting the presence of a contiguous population at an even larger scale, presumably by exchanging genes mainly between neighbours. We discuss the implications of these findings in terms of management of ship rats to protect native biodiversity.
Similar content being viewed by others
References
Abdelkrim J, Pascal M, Calmet C, Samadi S (2005a) Importance of assessing population genetic structure prior to eradication of invasive species: examples from insular Rattus norvegicus populations. Conserv Biol 19:1509–1518
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
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 21:719–730
Abdelkrim J, Pascal M, Samadi S (2009) Genetic structure and functionning of alien ship rat populations from a Corsican micro-insular complex. Biol Invasions 11(3):473–482
Amori G, Clout M (2003) Rodents on islands: a conservation challenge. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM (eds) Rats, mice and people: rodent biology and management. Australian Centre for International Agricultural Research, Canberra, pp 63–68
Atkinson IAE (1973) Spread of the ship rat (Rattus r. rattus L.) in New Zealand. J R Soc N Z 3:457–472
Bell BD (1978) The Big South Cape Island rat irruption. In: DP R, Atkinson IAE, Hay C (eds) The ecology and control of rodents in New Zealand nature reserves. Information series no. 4. Department of Land and Survey, Wellington, pp 33–40
Bomford M (1995) Eradication or control for vertebrate pests. Wildl Soc Bull 23:249–255
Carvalho DC, Oliveira DAA, Santos JE, Teske P, Beheregaray LB, Schneider H, Sampaio I (2009) Genetic characterization of native and introduced populations of the neotropical cichlid genus Cichla in Brazil. Genet Mol Biol 32:601–607
Cercueil A, Francois O, Manel S (2007) The genetical bandwidth mapping: a spatial and graphical representation of population genetic structure based on the Wombling method. Theor Popul Biol 71:332–341
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110
Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557
Didham RK, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496
Dieringer D, Schlötterer C (2002) Microsatellite analyser (MSA): a platform independent analysis tool for large data set. Mol Ecol Notes 3:167–169
Dowding JE, Murphy EC (1994) Ecology of ship rats (Rattus rattus) in Akauri (Agathis australis) forest in Northland, New Zealand. N Z J Ecol 18:19–28
Elliott G, Suggate R (2007) Operation Ark: 3-year progress report. Department of Conservation
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Forys AE, Allen CR (1999) Biological invasions and deletions: community change in south Florida. Biol Conserv 87:341–347
Gilabert A, Loiseau A, Duplantier JM, Rahelinirina S, Rahalison L, Chanteau S, Brouat C (2007) Genetic structure of black rat populations in a rural plague focus in Madagascar. Can J Zool 85:965–972
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html
Gratz N (1997) The burden of rodent-borne diseases in Africa south of the Sahara. Belg J Zool 127(Suppl):71–84
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Hoare JM, Adams LK, Bull LS (2007) Attempting to manage complex predatorprey interactions fails to avert imminent extinction of a threatened New Zealand skink population. J Wildl Manag 71:1576–1584
Howald G, Donlan CJ, Galvan JP, Russell JC, Parkes J, Samaniego A, Wang Y, Veitch D, Genovesi P, Pascal M, Saunders A, Tershy B (2007) Invasive rodent eradication on islands. Conserv Biol 21:1258–1268
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9(5):1322–1332
Innes J (2005) Ship rat. In: King CM (ed) The handbook of New Zealand mammals, 2nd edn. Oxford University Press, Melbourne, pp 187–203
Innes J, Hay R, Flux I, Bradfield P, Speed H, Jansen P (1999) Successfull recovery of North Island kokako Callaeas cinerea wilsoni populations, by adaptative management. Biol Conserv 87:201–214
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. Nat Genet 9:63–69
Le Roux J, Wieczorek AM (2009) Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Ann Appl Biol 154:1–17
Lowe S, Browne M, Boudjelas S (2000) 100 of the world’s worst invasive alien species. A selection from the global invasive species database. Invasive Species Specialist Group, Auckland, p 11
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Manel S, Berthoud F, Bellemain E, Gaudeul M, Luikart G, Swenson JE, Waits LP, Taberlet P (2007) A new individual-based spatial approach for identifying genetic discontinuities in natural populations. Mol Ecol 16:2031–2043
McClelland P, Tyree P (2002) Eratication: the clearance of Campbell Island. N Z Geogr 58:86–94
Miller MP (2005) Alleles in space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724
Mooney HA, Hobbs RJ (2000) Global change and invasive species: where do we go from here? In: Mooney HA, Hobbs JR (eds) Invasive species in a changing world. Island Press, Washington, DC, pp 425–434
Morgan DR, Nugent G, Warburton B (2006) Benefits and feasibility of local elimination of possum populations. Wildl Res 33:605–614
Morris KD (2002) The eradication of the black rat (Rattus rattus) on Barrow and adjacent islands off the north-west coast of Western Australia. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN SSC Invasive Species Specialist Group. IUCN, Switzerland and Cambridge, pp 219–225
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol 6:288–295
Pinceel J, Jordaens K, Van Houtte N, Bernon G, Backeljau T (2005) Population genetics and identity of an introduced terrestrial slug: Arion subfuscus s.l. in the North-East USA (Gastropoda, Pulmonata, Arionidae). Genetica 125:155–171
Prugnolle F, Theron A, Pointier JP, Jabbour-Zahab R, Jarne P, Durand P, De Meeus T (2005) Dispersal in a parasitic worm and its two hosts: consequences for local adaptation. Evol Int J Org Evol 59:296–303
Ramsay 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. Information series no. 4. Department of Land and Survey, Wellington, pp 89–95
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact test and ecumenicism. J Hered 86:248–249
Ricciardi A (2007) Are modern biological invasions an unprecedented form of global change? Conserv Biol 21:329–336
Rice WR (1989) Analizing tables of statistical tests. Evolution 43:223–225
Robertson BC, Gemmell NJ (2004) Defining eradication units in pest control programmes. J Appl Ecol 41:1032–1041
Rollins LA, Woolnough AP, Sherwin WB (2006) Population genetic tools for pest management: a review. Wildl Res 33:251–261
Russell JC, Abdelkrim A, Fewster RM (2009) Early colonisation population structure of a Norway rat island invasion. Biol Invasions 11:1557–1567
Sanders NJ, Gotelli NJ, Heller NE, Gordon DM (2003) Community disassembly by an invasive species. Proc Natl Acad Sci 100:2474–2477
Segelbacher G, Manel S, Tomiuk J (2008) Temporal and spatial analyses disclose consequences of habitat fragmentation on the genetic diversity in capercaillie (Tetrao urogallus). Mol Ecol 17:2356–2367
Simberloff D (1996) Impacts of introduced species in the United-States. Consequences 2:13–22
Sinclair ARE, Innes J, Bradfield P (2006) Making endangered species safe: the case of the kokako of North Island, New Zealand. N Z J Ecol 30:121–130
Spencer PBS, Hampton JO (2005) Illegal translocation and genetic structure of feral pigs in western Australia. J Wildl Manag 69:377–384
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
Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci 97:5948–5953
Vitousek PM, D’antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
Acknowledgements
We thank Dr Rachel Fewster and Dr Murray Efford for initiating this project and for helpful comments on the manuscript. We also thank Dr Michael Schwartz and three anonymous reviewers who provided comments and suggestions that greatly improved the manuscript. We thank Joelle Taillon, Richard Ball and Brian Karl who completed most of the fieldwork. We also thank Dr Gary Bramley, Richard Lee and Ian Wilson (Puketi Forest Trust) for their help. A permit for sample collection (NO-17635-RES) was provided by the Department of Conservation with the help of Donna Stuthridge. This work was funded by the Foundation for Research Science and Technology (Landcare Research contract numbers C09X0506 and C09X0909).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Abdelkrim, J., Byrom, A.E. & Gemmell, N.J. Fine-scale genetic structure of mainland invasive Rattus rattus populations: implications for restoration of forested conservation areas in New Zealand. Conserv Genet 11, 1953–1964 (2010). https://doi.org/10.1007/s10592-010-0085-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0085-9