Biological Invasions

, Volume 14, Issue 6, pp 1111–1125

‘Invasional meltdown’: evidence for unexpected consequences and cumulative impacts of multispecies invasions

Original Paper

Abstract

Empirical support for ‘invasional meltdown’, where the presence of one invading species facilitates another and compounds negative impacts on indigenous species, is equivocal with few convincing studies. In Ireland, the bank vole was introduced 80 years ago and now occupies a third of the island. The greater white-toothed shrew arrived more recently within the invasive range of the bank vole. We surveyed the abundance of both invasive species and two indigenous species, the wood mouse and pygmy shrew, throughout their respective ranges. The negative effects of invasive on indigenous species were strong and cumulative bringing about species replacement. The greater white-toothed shrew, the second invader, had a positive and synergistic effect on the abundance of the bank vole, the first invader, but a negative and compounding effect on the abundance of the wood mouse and occurrence of the pygmy shrew. The gradual replacement of the wood mouse by the bank vole decreased with distance from the point of the bank vole’s introduction whilst no pygmy shrews were captured where both invasive species were present. Such interactions may not be unique to invasions but characteristic of all multispecies communities. Small mammals are central in terrestrial food webs and compositional changes to this community in Ireland are likely to reverberate throughout the ecosystem. Vegetation composition and structure, invertebrate communities and the productivity of avian and mammalian predators are likely to be affected. Control of these invasive species may only be effected through landscape and habitat management.

Keywords

Impacts Interspecific competition Island populations Invasional meltdown Multiple invasions Small mammal community 

References

  1. Adams MJ, Pearl CA, Bury RB (2003) Indirect facilitation of an anuran invasion by non-native fishes. Ecol Lett 6:343–351CrossRefGoogle Scholar
  2. Adler GH, Levins R (1994) The island syndrome in rodent populations. Q Rev Biol 69:473–490PubMedCrossRefGoogle Scholar
  3. Akaike H (1983) Information measure and model selection. Bull Int Statist Inst 50:277–291Google Scholar
  4. Andrews P, O’Brien EM (2000) Climate, vegetation, and predictable gradients in mammal species richness in southern Africa. J Zool 251:205–231CrossRefGoogle Scholar
  5. Bell SS, White A, Sherratt JA, Boots M (2009) Invading with biological weapons: the role of shared disease in ecological invasion. Theor Ecol 2:53–66CrossRefGoogle Scholar
  6. Bergstedt B (1965) Distribution, reproduction, growth and dynamics of the rodent species Clethrionomys glareolus (Schreber), Apodemus flavicollis (Melchior) and Apodemus sylvaticus (Linne) in southern Sweden. Oikos 16:132–160CrossRefGoogle Scholar
  7. Bever K (1983) Zur Nahrung der Hausspitzmaus, Crocidura russula (Hermann 1780). Saugetier Mittl 31:13–26Google Scholar
  8. Birkan M (1968) Repartition ecologique et dynamique des populations d’Apodemus sylvaticus et Clethrionomys glareolus en Pinede a Rambouillet. La Terre et laVie 3:231–273Google Scholar
  9. Bohn T, Amundsen P, Sparrow A (2008) Competitive exclusion after invasion? Biol Inv 10:359–368CrossRefGoogle Scholar
  10. Boinski S, Kauffman L, Ehmke E, Schet S, Vreedzaam A (2005) Dispersal patterns among three species of squirrel monkeys (Saimiri oerstedii, S.boliviensis and S. sciureus): 1. Divergent costs and benefits. Behaviour 142:525–632CrossRefGoogle Scholar
  11. Booth GD, Niccolucci MJ, Schuster EG (1994) Identifying proxy sets in multiple linear regression: an aid to better coefficient interpretation. Research paper INT-470. United States Department of Agriculture Forest Service Ogden. USAGoogle Scholar
  12. Borroto-Paez R (2009) Invasive mammals in Cuba: an overview. Biol Inv 11:2279–2290CrossRefGoogle Scholar
  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  14. Courchamp F, Chapuis J-L, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383PubMedCrossRefGoogle Scholar
  15. Crawley M (1970) Some population dynamics of the Bank vole, Clethrionomys glareolus and the Wood mouse, Apodemus sylvaticus in mixed woodland. J Zool 160:71–89CrossRefGoogle Scholar
  16. De Jonge G, Dienske H (1979) Habitat and interspecific displacement of small mammals in the Netherlands. Neth J Zool 29:177–214CrossRefGoogle Scholar
  17. Eccard JA, Ylonen H (2003) Interspecific competition in small rodents: from populations to individuals. Evol Ecol 17:423–440CrossRefGoogle Scholar
  18. EEA (2000) CORINE land cover 2000. European Environment Agency. Available from http://www.eea.europa.eu/publications/COR0-landcover
  19. Ellenbroek FJM (1980) Interspecific competition in the shrews Sorex araneus and Sorex minutus (Soricidae, Insectivora): a population study of the Irish pygmy shrew. J Zool 192:119–136CrossRefGoogle Scholar
  20. Evans FC (1942) Studies of a small mammal population in Bagley Wood, Berkshire. J Anim Ecol 11:182–197CrossRefGoogle Scholar
  21. Fairley JS (1982) The muskrat in Ireland. Irish Nat J 20:405–411Google Scholar
  22. Fairley JS, Jones JM (1976) A woodland population of small rodents (Apodemus sylvaticus (L.) and Clethrionomys glareolus Schreber) at Adare, Co.Limerick. P Roy Irish Acad B 76:323–336Google Scholar
  23. Fasola M, Canova L (2000) Asymmetrical competition between the bank vole and the wood mouse, a removal experiment. Acta Theriol 45:353–365Google Scholar
  24. Fons R (1972) La musaraigne musette Crocidura russula (Hermann 1780. Sci Nat 112:23–28Google Scholar
  25. Fox BJ, Fox MD (2000) Factors determining mammal species richness on habitat islands and isolates: habitat diversity, disturbance, species interactions and guild assembly rules. Global Ecol Biogeog 9:19–37CrossRefGoogle Scholar
  26. Gosling LM, Baker SM (1987) Planning and monitoring an attempt to eradicate coypus in Britain. Symp Zool Soc 58:99–113Google Scholar
  27. Grainger JP, Fairley JS (1978) Studies on the biology of the pygmy shrew Sorex minutus in the west of Ireland. J Zool 186:109–141CrossRefGoogle Scholar
  28. Greenwood PJ (1978) Timing of the activity of the bank vole (Clethrionomys glareolus) and the wood mouse (Apodemus sylvaticus) in a deciduous woodland. Oikos 31:123–127CrossRefGoogle Scholar
  29. Hansson L (1971) Small rodent food, feeding and population dynamics. Oikos 22:183–198CrossRefGoogle Scholar
  30. Harris DB (2009) Review of negative effects of introduced rodents on small mammals on islands. Biol Inv 11:1611–1630CrossRefGoogle Scholar
  31. Harris S, Yalden DW (eds) (2008) Mammals of the British Isles: Handbook, 4th edn. Tthe Mammal Society, Southampton, UKGoogle Scholar
  32. Holisova V, Obrtel R (1980) Food resource partitioning among four myomorph rodent populations coexisting in a spruce forest. Folia Zool 29:193–207Google Scholar
  33. Huitu O, Norrdahl K, Korpimaki E (2003) Landscape effects on temporal and spatial properties of vole population fluctuations. Oecologia 135:209–220PubMedGoogle Scholar
  34. Kelt DA, Taper ML, Meserve PL (1995) Assessing the impact of competition on community assembly—a case study using small mammals. Ecology 76:1283–1296CrossRefGoogle Scholar
  35. Kikkawa J (1964) Movement, activity and distribution of the small rodents Clethrionomys glareolus and Apodemus sylvaticus in woodland. J Anim Ecol 33:259–299CrossRefGoogle Scholar
  36. King CM, Foster S, Miller S (2011) Invasive rats in Britain and new Zealand: sam species, different outcomes. J Zool 285:172–179Google Scholar
  37. Leisenjohann M, Liesenjohann T, Trebaticka F, Haapakoski M, Sundell J, Ylonen H, Eccard J (2011) From interference to predation: type and effects of direct interspecific interactions of small mammals. Behav Ecol Sociobiol. doi:10.1007/s00265-011-1217-z
  38. Liu L, Yip PS (2003) Estimating population size in proportional trapping- removal models. Stat Sinica 13:243–254Google Scholar
  39. Lundy M, Montgomery I (2010) A multi-scale analysis of the habitat associations of European otter and American mink and the implications for farm scale conservation schemes. Biodiversity Conserv 19:3849–3859CrossRefGoogle Scholar
  40. Marnell F, Kingston N, Looney D (2009) Ireland red list No. 3: Terrestrial Mammals, National Parks and Wildlife Service, Department of the Environment. Heritage and Local Government, DublinGoogle Scholar
  41. McAlpine CA, Rhodes JR, Callaghan JG (2006) The importance of forest area and configuration relative to local habitat factors for conserving forest mammals: a case study of koalas in Queensland, Australia. Biol Conserv 132:153–165CrossRefGoogle Scholar
  42. McCormick F (1999) Early evidence for wild animals in Ireland. In: Benecke N (ed) The holocene history of the European vertebrate fauna: modern aspects of research. Verlag Marie Leidorf GmbH, Rahden, Germany, pp 355–371Google Scholar
  43. Meehan JM (2005) Range expansion of the bank vole Clethrionomys glareolus (Schreber 1780) in Ireland: habitat use by sympatric bank voles and wood mice Apodemus sylvaticus (Kamp 1829). Unpublished PhD thesis, University College CorkGoogle Scholar
  44. Meharg MJ, Montgomery WI, Dunwoody T (1990) Trophic relationships of common frog (Rana temporaria) and pigmy shrew (Sorex minutus) in Ireland. J Zool 222:1–17CrossRefGoogle Scholar
  45. Mermod C (1969) Ecologie et dynamique des populations de trios rongeurs sylvicoles. Mammalia 33:1–57CrossRefGoogle Scholar
  46. Miller RS (1955) Activity rhythms in the wood mouse Apodemus sylvaticus and bank vole Clethrionomys glareolus. P Zool Soc Lond 125:505–519CrossRefGoogle Scholar
  47. Montgomery SSJ, Montgomery WI (1989) Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus(Rodentia: Muridae). Parasitology 98:145–150PubMedCrossRefGoogle Scholar
  48. Morris DW (2005) On the roles of time, space and habitat in a boreal small mammal assemblage: predictably stochastic assembly. Oikos 109:223–238CrossRefGoogle Scholar
  49. Nupp TE, Swihart RK (2000) Landscape-level correlates of small mammal assemblages in forest fragments of farmland. J Mammal 81:512–526CrossRefGoogle Scholar
  50. Orrock JL, Pagels JF, McShea WJ, Harper EK (2000) Predicting presence and abundance of a small mammal species: the effect of scale and resolution. Ecol Appl 10:1356–1366CrossRefGoogle Scholar
  51. Otis DL, Burnham KP, White GC, Anderson DR (1978) Statistical inference from capture data on closed animal populations, Wildlife Monographs 62 pp 135 The Wildlife Society, Washington, DCGoogle Scholar
  52. Panzacchi M, Lindell JDC, Melis C, Odden M, Odden J, Gorini L, Anderson R (2010) Effect of land-use on small mammal abundance and diversity in a forest-farmland mosaic landscape in south eastern Norway. Forest Ecol Manag 259:1536–1545CrossRefGoogle Scholar
  53. Pascal M, Lorvelec O, Bioret F, Yésou P, Simberloff D (2009) Habitat use and potential interactions between the house mouse and lesser white-toothed shrew on an island undergoing habitat restoration. Acta Theriol 54:39–49CrossRefGoogle Scholar
  54. Pianka ER (1974) Niche overlap and diffuse competition. Proc Natl Acad Sci USA 71:2141–2145PubMedCrossRefGoogle Scholar
  55. Preece RC, Coxon P, Robinson JE (1986) New biostratigraphic evidence of the post-glacial colonisation of Ireland and for Mesolithic forest disturbance. J Biogeog 13:487–509CrossRefGoogle Scholar
  56. Probert BL, Litvaitis JA (1996) Behavioral interactions between invading and endemic lagomorphs: implications for conserving a declining species. Biol Conserv 76:289–295CrossRefGoogle Scholar
  57. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  58. Reid N (2010) European hare (Lepus europaeus) invasion ecology; implications for the conservation of the endemic Irish hare (Lepus timidus hibernicus). Biol Inv 13(3):559–569Google Scholar
  59. Reid N, Montgomery WI (2007) Is naturalisation of the brown hare in Ireland a threat to the endemic Irish hare? Biol Environ 107(3):129–138Google Scholar
  60. Rushton SP, Lurz PWW, Gurnell J, Fuller R (2000) Modelling the spatial dynamics of parapoxvirus disease in red and grey squirrels: a possible cause of decline in the red squirrel in the UK? J Appl Ecol 37:997–1012CrossRefGoogle Scholar
  61. Searle JB (2008) The colonisation of Ireland by mammals. In: Davenport JL, Sleeman DP, Woodman PC (eds) Special supplement to the Irish Naturalists’ Journal, pp 109–115Google Scholar
  62. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919PubMedCrossRefGoogle Scholar
  63. Simberloff D (2009) Rats are not the only introduced rodents producing ecosystem impacts on islands. Biol Inv 11:1735–1742CrossRefGoogle Scholar
  64. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Inv 5:179–192CrossRefGoogle Scholar
  65. Smal CM, Fairley JS (1981) Energy consumption of small rodent populations in two Irish woodland ecosystems. Acta Theriol 26:449–458Google Scholar
  66. Smal CM, Fairley JS (1982) The dynamics and regulation of small rodent populations in the woodland ecosystems of Killarney, Ireland. J Zool 196:1–30CrossRefGoogle Scholar
  67. Smith AP, Quinn DG (1996) Patterns and causes of extinction and decline in Australian conilurine rodents. Biol Conserv 77:243–267CrossRefGoogle Scholar
  68. Southern HN, Lowe VPW (1968) Predation by Tawny owls (Strix aluco) on Bank voles (Clethrionomys glareolus) and Wood mice (Apodemus sylvaticus). J Zool 198:83–102CrossRefGoogle Scholar
  69. St Clair JJH (2011) The impacts of invasive rodents on island invertebrates. Biol Conserv 144:68–81CrossRefGoogle Scholar
  70. 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
  71. Stuart P, Sleeman DP (2006) Fleas from bank voles (Clethrionomys glareolus Schreber) near Foynes, Co. Limerick. Irish Nat J 28:221Google Scholar
  72. Stuart P, Mirimin L, Cross TF, Sleeman DP, Buckley NJ, Telfer S, Birtles RJ, Kotlik P, Searle JB (2007) The origin of Irish bank voles Clethrionomys glareolus assessed by mitochondrial DNA analysis. Irish Nat J 28:440–446Google Scholar
  73. Tanton MT (1969) The estimation and biology of populations of the bank vole (Clethrionomys glareolus (Schr.)) and Wood mouse (Apodemus sylvaticus (L.)). J Anim Ecol 38:511–529CrossRefGoogle Scholar
  74. Telfer S, Bennett M, Bown K, Cavanagh R, Crespin L, Hazel S, Jones T, Begon M (2002) The effects of cowpox virus on survival in natural rodent populations: increases and decreases. J Anim Ecol 71:558–568CrossRefGoogle Scholar
  75. Telfer S, Bown KJ, Sekules R, Begon M, Hayden T, Birtles R (2005a) Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130:661–668PubMedCrossRefGoogle Scholar
  76. Telfer S, Bennett M, Bown K, Carslake D, Cavanagh R, Hazel S, Jones T, Begon M (2005b) infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents. Oikos 109:317–322CrossRefGoogle Scholar
  77. Torchin ME, Laverty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nat Lond 421:628–630CrossRefGoogle Scholar
  78. Tosh DG, Lusby J, Montgomery WI, O’Halloran J (2008) First record of greater white-toothed shrew Crocidura russula in Ireland. Mammal Rev 38:321–326CrossRefGoogle Scholar
  79. Veitch CR, Clout MN (2002) Turning the tide: the eradication of invasive species. In: Proceedings of the international conference on eradication of Island Invasives. IUCN, Gland, Switzerland and CambridgeGoogle Scholar
  80. Vibe-Petersen S, Leirs H, De Bruyn L (2006) Effects of predation and dispersal on Mastomys natalensis population dynamics in Tanzanian maize fields. J Anim Ecol 75:213–220PubMedCrossRefGoogle Scholar
  81. Wardles DA, Bardgett RD, Callaway RM, Van der Putten W (2011) Terrestrial ecosystem response to species gains and losses. Science 332:1273–1277CrossRefGoogle Scholar
  82. Warren CR (2007) Perspectives on the ‘alien’ versus ‘native’ species debate: a critique of concepts, language and practice. Prog Human Geogr 31:427–446CrossRefGoogle Scholar
  83. Watts CHS (1968) The foods eaten by wood mice (Apodemus sylvaticus) and Bank voles (Clethrionomys glareolus) in Wytham Woods, Berkshire. J Anim Ecol 37:25–41CrossRefGoogle Scholar
  84. White PCL, Harris S (2002) Economic and environmental costs of alien vertebrate species in Britain. In: Pimentel D (ed) Biological invasions: economic and environmental costs of alien plant, animal and microbe species. CRC Press, Boca Raton, FLGoogle Scholar
  85. Yalden D (1999) The history of British mammals. Poyser Natural History, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • W. Ian Montgomery
    • 1
  • Mathieu G. Lundy
    • 1
  • Neil Reid
    • 1
  1. 1.School of Biological Sciences, Queen’s University BelfastBelfastNorthern Ireland, UK

Personalised recommendations