, Volume 172, Issue 3, pp 737–749 | Cite as

Anthropogenic subsidies mitigate environmental variability for insular rodents

  • Lise RuffinoEmail author
  • James Russell
  • Eric Vidal
Population ecology - Original research


The exogenous input of nutrients and energy into island systems fuels a large array of consumers and drives bottom-up trophic cascades in island communities. The input of anthropogenic resources has increased on islands and particularly supplemented non-native consumers with extra resources. We test the hypothesis that the anthropogenic establishments of super-abundant gulls and invasive iceplants Carpobrotus spp. have both altered the dynamics of an introduced black rat Rattus rattus population. On Bagaud Island, two habitats have been substantially modified by the anthropogenic subsidies of gulls and iceplants, in contrast to the native Mediterranean scrubland with no anthropogenic inputs. Rats were trapped in all three habitats over two contrasting years of rainfall patterns to investigate: (1) the effect of anthropogenic subsidies on rat density, age-ratio and growth rates, and (2) the role of rainfall variability in modulating the effects of subsidies between years. We found that the growth rates of rats dwelling in the non-subsidized habitat varied with environmental fluctuation, whereas rats dwelling in the gull colony maintained high growth rates during both dry and rainy years. The presence of anthropogenic subsidies apparently mitigated environmental stress. Age ratio and rat density varied significantly and predictably among years, seasons, and habitats. While rat densities always peaked higher in the gull colony, especially after rat breeding in spring, higher captures of immature rats were recorded during the second year in all habitats, associated with higher rainfall. The potential for non-native rats to benefit from anthropogenic resources has important implications for the management of similar species on islands.


Anthropogenic resources Mediterranean islands Population dynamics Rattus rattus Trophic subsidies 



We would like to thank all the people who help in the field and during laboratory work. We specially thank all the PCNP staff who enabled this long-term study on the natural reserve of Bagaud Island. Research was funded by the ‘Agence Nationale pour la Recherche’ (ANR) with program ‘ALIENS’. Funds were provided by a PhD fellowship granted by ‘Ecole Doctorale des Sciences de l’Environement’ to L.R., a postdoctoral fellowship granted by the New Zealand Foundation for Research, Science and Technology to J.C.R.

Supplementary material

442_2012_2545_MOESM1_ESM.doc (93 kb)
Supplementary material 1 (DOC 93 kb)


  1. Anderson WB, Polis GA (1999) Nutrient fluxes from water to land: seabirds affect plant nutrient status on the Gulf of California islands. Oecologia 118:324–332CrossRefGoogle Scholar
  2. Anderson WB, Wait DA, Stapp P (2008) Resources from another place and time: responses to pulses in a spatially subsidized system. Ecology 89:660–670PubMedCrossRefGoogle Scholar
  3. Aplin KP, Brown PR, Jacob J, Krebs CJ, Singleton GR (2003) Field methods for rodent studies in Asia and the Indo-Pacific. ACIAR Monograph 100. ACIAR, CanberraGoogle Scholar
  4. Atkinson AI (1985) The spread of commensal species of Rattus to Oceanic Islands and their effects on island avifaunas. In: Moors RJ (ed) Conservation of island birds. ICBP Technical Publication No. 3, Cambridge, pp 35–81Google Scholar
  5. Banks PB, Dickman CR (2000) Effects of winter food supplementation on reproduction, body mass, and numbers of small mammals in montane Australia. Can J Zool 78:1775–1783CrossRefGoogle Scholar
  6. Barrett K, Anderson WB, Wait DA, Grismer LL, Polis GA, Rose MD (2005) Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos 19:145–153CrossRefGoogle Scholar
  7. Borchers DL, Efford MG (2008) Spatially explicit maximum likelihood methods for capture-recapture studies. Biometrics 64:377–385PubMedCrossRefGoogle Scholar
  8. Bourgeois K (2002) Analysis of the role of vertebrates in the dissemination and germination of Carpobrotus ssp. (Aizoaceae), invasive alien plants on the Mediterranean coast. Diploma, University of Aix-MarseilleGoogle Scholar
  9. Bourgeois K, Suehs CM, Vidal E, Médail F (2005) Invasional meltdown potential: facilitations between introduced plants and mammals on French Mediterranean islands. Ecoscience 12:248–256CrossRefGoogle Scholar
  10. Brown JH, Ernest SKM (2002) Rain and rodents: complex dynamics of desert consumers. Bioscience 52:979–987CrossRefGoogle Scholar
  11. Catenazzi A, Donnelli MA (2007) The Ulva connection: marine algae subsidize terrestrail predators in coastal Peru. Oikos 116:75–86CrossRefGoogle Scholar
  12. Cheylan G (1988) Les adaptations écologiques de Rattus rattus à la survie dans les îlots méditerranéens (Provence et Corse). Bull Ecol 19:417–426Google Scholar
  13. Clark DA (1981) Foraging patterns of black rats across a desert-montane forest gradient in the Galapagos islands. Biotropica 13:182–184CrossRefGoogle 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. Doonan TJ, Slade NA (1995) Effects of supplemental food on population dynamics of cotton rats, Sigmodon hispidus. Ecology 76:814–826CrossRefGoogle Scholar
  16. Efford MG, Borchers DL, Byrom AE (2009) Density estimation by spatially explicit capture–recapture: likelihood-based methods. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Springer, Berlin, pp 255–269CrossRefGoogle Scholar
  17. Eifler MA, Slade NA, Doonan TJ (2003) The effect of supplemented food on the growth rates of neonatal, young, and adult cotton rats (Sigmodon hispidus) in northeastern Kansas, USA. Acta Oecol 24:187–193CrossRefGoogle Scholar
  18. 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
  19. Ellis JC, Farina JM, Witman JD (2006) Nutrient transfer from water to land: the case of gulls and cormorants of the Gulf of Maine. J Anim Ecol 75:565–574PubMedCrossRefGoogle Scholar
  20. Ernest SKM, Brown JH, Parmenter RR (2000) Rodents, plants, and precipitation: spatial and temporal dynamics of consumers and resources. Oikos 88:470–482CrossRefGoogle Scholar
  21. Farina JM, Salazar S, Wallem KP, Witman JD, Ellis JC (2003) Nutrient exchanges between marine and terrestrial ecosystems: the case of the Galapagos sea lion Zalophus wollebaecki. J Anim Ecol 72:873–887CrossRefGoogle Scholar
  22. Faugier C, Pascal M (2006) Insectivores et rongeurs de France: le rat noir Rattus rattus Linné 1758. Arvicola 17:42–53Google Scholar
  23. Hart DR, Chute AS (2009) Estimating von Bertalanffy growth parameters from growth increment data using a linear mixed-effects model, with an application to the sea scallop Placopecten magellanicus. ICES J Mar Sci 66:2165–2175CrossRefGoogle Scholar
  24. Holt RD, Barfield M (2003) Impacts of temporal variation on apparent competition and coexistence in open ecosystems. Oikos 101:49–58CrossRefGoogle Scholar
  25. Hulme PE (2004) Invasions, islands and impacts: a Mediterranean perspective. In: Fernandez Palacios JM (ed) Island Ecology. Asociación Española de Ecología Terrestre. La Laguna, Spain, pp 337–361Google Scholar
  26. Iason GR, Duck CD, Clutton TH (1986) Grazing and reproductive success of red deer: the effect of local enrichment by gull colonies. J Anim Ecol 55:507–515CrossRefGoogle Scholar
  27. King CM, Moller H (1997) Distribution and responses of rats R. rattus and R. exulans to seedfall in New Zealand beech forests. Pac Conserv Biol 3:143–155Google Scholar
  28. King CM, Innes JG, Gleeson D, Fitzgerald N, Winstanley T, O’Brien B, Bridgman L, Coxt N (2011) Reinvasion by ship rats (Rattus rattus) of forest fragments after eradication. Biol Invasions 13:2391–2408CrossRefGoogle Scholar
  29. Lin Y-TK, Batzli GO (2001) The influence of habitat quality on dispersal, demography, and population dynamics of voles. Ecol Monog 71:245–275CrossRefGoogle Scholar
  30. Madsen T, Shine R (1999) Impacts of temporal variation on apparent competition and coexistence in open ecosystems. Aust J Ecol 24:80–89CrossRefGoogle Scholar
  31. Marczak LB, Thompson RM, Richardson JS (2007) Meta-analysis: trophic level, habitat and productivity shape the food web effects of resource subsidies. Ecology 88:140–148PubMedCrossRefGoogle Scholar
  32. Markwell TJ, Daugherty CH (2002) Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience 9:293–299Google Scholar
  33. Martin JL, Thibault JC, Bretagnolle V (2000) Black rats, island characteristics and colonial nesting birds in the Mediterranean: consequences of an ancient introduction. Conserv Biol 14:1452–1466Google Scholar
  34. McCann KS, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798CrossRefGoogle Scholar
  35. Meserve PL, Kelt DA, Mylstead WB, Guttiérez JR (2003) Thirteen years of shifting top-down and bottom-up control. Bioscience 53:633–646CrossRefGoogle Scholar
  36. Millar JS (1978) Energetics of reproduction in Peromyscus leucopus: the cost of lactation. Ecology 59:1055–1061CrossRefGoogle Scholar
  37. Orgeas J, Vidal E, Ponel P (2003) Colonial seabirds change beetle assemblages on a Mediterranean island. Ecoscience 10:38–44Google Scholar
  38. Paetzold A, Lee M, Post DM (2008) Marine resource flows to terrestrial arthropod predators on a temperate island: the role of subsidies between systems of similar productivity. Oecologia 157:653–659PubMedCrossRefGoogle Scholar
  39. Polis GA, Hurd SD (1996) Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat 147:396–423CrossRefGoogle Scholar
  40. Polis GA, Holt RD, Menge BA, Winemiller KO (1996) Allochthonous input across habitats, subsidized consumers, and apparent trophic cascades: examples from the ocean-land interface. In: Polis GA, Winemiller K (eds) Food webs. Integration of patterns and dynamics. Chapman and Hall, New York, pp 275–285CrossRefGoogle Scholar
  41. Polis GA, Anderson WB, Holt RD (1997a) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316CrossRefGoogle Scholar
  42. Polis GA, Hurd SD, Jackson CT, Sanchez-Pinero F (1997b) El Niño effects on the dynamics and control of a terrestrial island ecosystem in the Gulf of California. Ecology 78:1884–1897Google Scholar
  43. Polis GA, Sanchez-Pinero F, Stapp P, Rose M, Anderson WB (2004) Trophic flows from water to land: marine input affects food webs of islands and coastal ecosystems worldwide. In: Polis GA, Power ME, Huxel GR (eds) Food webs at the landscape level. Chicago University Press, Chicago, pp 200–216Google Scholar
  44. Randolph PA, Randolph JC, Mattingly K, Foster MM (1977) Energy cost of reproduction in the cotton rat, Sigmodon hispidus. Ecology 58:31–45CrossRefGoogle Scholar
  45. Rose MD, Polis GA (1998) The distribution and abundance of coyotes: the effects of allochthonous food subsidies from the sea. Ecology 79(33):998–1007CrossRefGoogle Scholar
  46. Ruffino L (2010) Ecologie, dynamique de population, comportement et impact d’un rongeur introduit Rattus rattus sur les îles de Méditerranée. PhD dissertation, Paul Cezanne University, Aix-en-ProvenceGoogle Scholar
  47. Ruffino L, Vidal E (2012) Importance de la ressource griffe de sorcière Carpobrotus spp. pour les rats noirs Rattus rattus de l’île de Bagaud (Parc national de Port Cros, Var, France). Travaux Scientifiques du Parc National de Port-Cros 26:173–193Google Scholar
  48. Ruffino L, Bourgeois K, Vidal E, Duhem C, Paracuellos M, Escribano F, Sposimo P, Baccetti N, Pascal M, Oro D (2009) Invasive rats and seabirds: a review after 2,000 years of an unwanted coexistence on Mediterranean islands. Biol Invasions 11:1631–1651CrossRefGoogle Scholar
  49. Ruffino L, Russell JC, Pisanu B, Caut S, Vidal E (2011) Low individual-level diet plasticity in an island invasive generalist forager. Pop Ecol 53:535–548CrossRefGoogle Scholar
  50. Ruscoe WA, Wilson D, McElrea L, McElrea G, Richardson SJ (2004) A house mouse (Mus musculus) population eruption in response to rimu (Dacrydium cupressinum) seedfall in southern New Zealand. NZ J Ecol 28:259–265Google Scholar
  51. Russell JC (2011) Indirect effects of introduced predators on seabird islands. In: Mulder CPH, Anderson WB, Towns DR, Bellingham PJ (eds) Seabird Islands: ecology, invasion, and restoration. Oxford University Press, New York, pp 261–279Google Scholar
  52. Russell JC, Ruffino L (2012) The influence of spatio-temporal resource fluctuations on insular rat population dynamics. Proc R Soc Lond B 279:767–774CrossRefGoogle Scholar
  53. Russell JC, Faulquier L, Tonione MA (2011a) Rat invasion of Tetiaroa atoll, French Polynesia. In: Veitch CR, Clout MN, Towns DR (eds) Island invasives: eradication and management. IUCN, Gland, pp 118–123Google Scholar
  54. Russell JC, Ringler D, Trombini A, Le Corre M (2011b) The island syndrome and population dynamics of introduced rats. Oecologia 167:667–676PubMedCrossRefGoogle Scholar
  55. Sanchez-Piñero F, Polis GA (2000) Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81:3117–3132Google Scholar
  56. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919PubMedCrossRefGoogle Scholar
  57. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  58. Stapp P, Polis GA (2003a) Influence of pulsed resources and marine subsidies on insular rodent populations. Oikos 102:111–123CrossRefGoogle Scholar
  59. Stapp P, Polis GA (2003b) Marine resources subsidize insular rodent populations in the Gulf of California, Mexico. Oecologia 134:496–504PubMedGoogle Scholar
  60. Stapp P, Polis GA, Sanchez-Pinero F (1999) Stable isotopes reveal strong marine and El Niño effects on island food webs. Nature 401:467–469CrossRefGoogle Scholar
  61. 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
  62. Suehs CM, Affre L, Médail F (2004) Invasion dynamics of two alien Carpobrotus (Aizoaceae) taxa on a Mediterranean island: I. Genetic diversity and introgression. Heredity 92:31–40PubMedCrossRefGoogle Scholar
  63. Vidal E, Medail F, Tatoni T (1998a) Is the yellow-legged gull a superabundant bird species in the Mediterranean? Impact on fauna and flora, conservation measures and research priorities. Biodivers Conserv 7:1013–1026CrossRefGoogle Scholar
  64. Vidal E, Médail F, Thierry T, Roche P, Vidal P (1998b) Impact of gull colonies on the flora of the Riou archipelago (Mediterranean islands of South-East France). Biol Conserv 84:235–243CrossRefGoogle Scholar
  65. Wait DA, Audrey DP, Anderson WB (2005) Seabird guano influences on desert islands: soil chemistry and herbaceous species richness and productivity. J Arid Environ 60:681–695CrossRefGoogle Scholar
  66. Wolfe KM, Mills HR, Garkaklis MJ, Bencini R (2004) Post-mating survival in a small marsupial in associated with nutrient input from seabirds. Ecology 85:1740–1746CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Biology, Section of EcologyUniversity of TurkuTurkuFinland
  2. 2.IMBE, UMR CNRS7273/IRD237/Aix-Marseille UniversityAix-en-Provence Cédex 04France
  3. 3.School of Biological Sciences and Department of StatisticsUniversity of AucklandAucklandNew Zealand
  4. 4.IMBE, UMR CNRS 7263/IRD 237/AMU Centre IRD de NoumeaNoumea cedexFrance

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