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Biological Invasions

, Volume 18, Issue 7, pp 1923–1938 | Cite as

A synergistic trio of invasive mammals? Facilitative interactions among beavers, muskrats, and mink at the southern end of the Americas

  • Ramiro D. CregoEmail author
  • Jaime E. Jiménez
  • Ricardo Rozzi
Original Paper

Abstract

With ecosystems increasingly having co-occurring invasive species, it is becoming more important to understand invasive species interactions. At the southern end of the Americas, American beavers (Castor canadensis), muskrats (Ondatra zibethicus), and American mink (Neovison vison), were independently introduced. We used generalized linear models to investigate how muskrat presence related to beaver-modified habitats on Navarino Island, Chile. We also investigated the trophic interactions of the mink with muskrats and beavers by studying mink diet. Additionally, we proposed a conceptual species interaction framework involving these invasive species on the new terrestrial community. Our results indicated a positive association between muskrat presence and beaver-modified habitats. Model average coefficients indicated that muskrats preferred beaver-modified freshwater ecosystems, compared to not dammed naturally flowing streams. In addition, mammals and fish represented the main prey items for mink. Although fish were mink’s dominant prey in marine coastal habitats, muskrats represented >50 % of the biomass of mink diet in inland environments. We propose that beavers affect river flow and native vegetation, changing forests into wetlands with abundant grasses and rush vegetation. Thus, beavers facilitate the existence of muskrats, which in turn sustain inland mink populations. The latter have major impacts on the native biota, especially on native birds and small rodents. The facilitative interactions among beavers, muskrats, and mink that we explored in this study, together with other non-native species, suggest that an invasive meltdown process may exist; however further research is needed to confirm this hypothesis. Finally, we propose a community-level management to conserve the biological integrity of native ecosystems.

Keywords

Cape Horn Ecosystem changes Invasive meltdown Invasive species interactions Sub-Antarctic Magellanic forests 

Notes

Acknowledgments

We thank Matías Barceló, Nicolás Carro, Gabriel Gómez, Simón Castillo, Ana Piñeiro, Fernando Saldivia, Rocio Jara, Omar Barroso, and Javier Rendoll for all their hard field work help. We appreciate the valuable support of Nicolas Soto and Cristian Soto to this project. We also thank Amy Wynia and two anonymous reviewers for their valuable comments that significantly improved this manuscript. Tamara Contador and the Omora Foundation provided support to this project, with access to the Wankara Laboratory facilities and insect identification. This study was financed by the Toulouse Graduate School Program at the University of North Texas (UNT), the Rufford Foundation, the Conservation Research and Education Opportunities International (CREOi), and the Institute of Ecology and Biodiversity of Chile (IEB; grants ICM P05-002 and Basal-CONICYT PFB-23). This study is a contribution of the Sub-Antarctic Biocultural Conservation Program, jointly coordinated by UNT in the US, and by IEB and the Universidad de Magallanes in Chile.

Supplementary material

10530_2016_1135_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 20 kb)

References

  1. Anderson CB, Rosemond AD (2007) Ecosystem engineering by invasive exotic beavers reduces in-stream diversity and enhances ecosystem function in Cape Horn, Chile. Oecologia 154:141–153CrossRefPubMedGoogle Scholar
  2. Anderson CB, Rozzi R, Torres-Mura JC, McGehee SM, Sherriffs MF, Schüttler E, Rosemond AD (2006a) Exotic vertebrate fauna in the remote and pristine Sub-Antarctic Cape Horn Archipelago, Chile. Biodivers Conserv 15:3295–3313CrossRefGoogle Scholar
  3. Anderson CB, Griffith CR, Rosemond AD, Rozzi R, Dollenz O (2006b) The effects of invasive North American beavers on riparian plant communities in Cape Horn, Chile: do exotic beavers engineer differently in Sub-Antarctic ecosystems? Biol Conserv 128:467–474CrossRefGoogle Scholar
  4. Anderson CB, Pastur GM, Lencinas MV, Wallem PK, Moorman MC, Rosemond AD (2009) Do introduced North American beavers Castor canadensis engineer differently in southern South America? An overview with implications for restoration. Mamm Rev 39:33–52CrossRefGoogle Scholar
  5. Angermeier PL, Karr JR (1994) Biological integrity versus biological diversity as policy directives. Bioscience 44:690–697CrossRefGoogle Scholar
  6. Artimo A (1960) The dispersal and acclimatization of the muskrat, Ondatra zibethicus (L.), in Finland. Pap Game Res 21:1–101Google Scholar
  7. Brzeziński M, Marzec M (2003) Correction factors used for estimating prey biomass in the diet of American mink Mustela vison. Acta Theriol 48:247–254CrossRefGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New YorkGoogle Scholar
  9. Chehébar C, Martín S (1980) Guía para el reconocimiento microscópico de los pelos de los mamíferos de la Patagonia. Acta Vertebr 16:247–291Google Scholar
  10. Connors LM, Groffman PM, Ostfeld RS (2000) Muskrat (Ondatra zibethicus) disturbance to vegetation and potential net nitrogen mineralization and nitrification rates in a freshwater tidal marsh. Am Midl Nat 143:53–63CrossRefGoogle Scholar
  11. Contador T, Kennedy JH, Rozzi R, Villarroel JO (2015) Sharp altitudinal gradients in Magellanic Sub-Antarctic streams: patterns along a fluvial system in the Cape Horn biosphere reserve (55°S). Polar Biol 38:1853–1866CrossRefGoogle Scholar
  12. Crawley M (2002) Statistical computing: an introduction to data analysis using S-Plus. Wiley, New YorkGoogle Scholar
  13. Crego RD, Jiménez JE, Soto C, Barroso O, Rozzi R (2014) Tendencias poblacionales del visón norteamericano invasor (Neovison vison) y sus principales presas nativas desde su arribo a isla Navarino, Chile. Boletín de la Red Latinoamericana para el Estudio de Especies Invasoras 4:4–18Google Scholar
  14. Crego RD, Jimenez JE, Rozzi R (2015) Expansión de la invasión del Visón Norteamericano (Neovison vison) en la Reserva de la Biosfera de Cabo de Hornos, Chile. Anales del Instituto de la Patagonia 43:157–162Google Scholar
  15. de Szalay FA, Cassidy W (2001) Effects of muskrat (Ondatra zibethicus) lodge construction on invertebrate communities in a Great Lakes coastal wetland. Am Midl Nat 146:300–310CrossRefGoogle Scholar
  16. Deferrari G (2007) Biología y ecomorfología de la rata almizclera en Tierra del Fuego. Tesis Doctoral, Universidad Nacional de La PlataGoogle Scholar
  17. Dunstone N (1993) The Mink. T and A D Poyser Ltd., LondonGoogle Scholar
  18. Eagle TC, Whitman JS (1987) Mink. In: Novak M, Baker JA, Obbard ME, Malloch B (eds) Wild furbearer management and conservation in North America. Ontario Ministry of Natural Resources, Toronto, pp 615–624Google Scholar
  19. Edwards NT, Otis DL (1999) Avian communities and habitat relationships in South Carolina piedmont beaver ponds. Am Midl Nat 141:158–171CrossRefGoogle Scholar
  20. Engeman RM, Whisson DA (2005) A visual method for indexing muskrat populations. Int Biodeterior Biodegradation 52:101–106CrossRefGoogle Scholar
  21. Glen AS, Atkinson R, Campbell KJ et al (2013) Eradicating multiple invasive species on inhabited islands: the next big step in island restoration? Biol Invasions 15:2589–2603CrossRefGoogle Scholar
  22. Gomez JJ, Gozzi AC, Macdonald DW et al (2010) Interactions of exotic and native carnivores in an ecotone, the coast of the Beagle Channel, Argentina. Polar Biol 33:1371–1378CrossRefGoogle Scholar
  23. Green PT, O’Dowd DJ, Abbott KL et al (2011) Invasional meltdown: invader–invader mutualism facilitates a secondary invasion. Ecology 92:1758–1768CrossRefPubMedGoogle Scholar
  24. Hayward J, Horton TR, Nuñez MA (2015) Ectomycorrhizal fungal communities coinvading with Pinaceae host plants in Argentina: Gringos bajo el bosque. New Phytol. doi: 10.1111/nph.13453 PubMedGoogle Scholar
  25. Heimpel GE, Frelich LE, Landis DA et al (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931CrossRefGoogle Scholar
  26. Hobbs RJ, Arico S, Aronson J et al (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15:1–7CrossRefGoogle Scholar
  27. Ibarra JT, Fasola L, Macdonald DW, Rozzi R, Bonacic C (2009) Invasive American mink Mustela vison in wetlands of the Cape Horn Biosphere Reserve, southern Chile: what are they eating? Oryx 43:87–90CrossRefGoogle Scholar
  28. Jackson MC (2015) Interactions among multiple invasive animals. Ecology 96:2035–2041CrossRefPubMedGoogle Scholar
  29. Jaksic FM, Iriarte JA, Jiménez JE, Martínez DR (2002) Invaders without frontiers: cross-border invasions of exotic mammals. Biol Invasions 4:157–173CrossRefGoogle Scholar
  30. Jiménez JE, Crego RD, Soto GE et al (2014) Potential impact of the alien American mink (Neovison vison) on Magellanic woodpeckers (Campephilus magellanicus) in Navarino Island, southern Chile. Biol Invasions 16:961–966CrossRefGoogle Scholar
  31. Johnson PTJ, Olden JD, Solomon CT, Vander Zanden MJ (2009) Interactions among invaders: community and ecosystem effects of multiple invasive species in an experimental aquatic system. Oecologia 159:161–170CrossRefPubMedGoogle Scholar
  32. Kuebbing SE, Nuñez MA (2014) Negative, neutral, and positive interactions among nonnative plants: patterns, processes and management implications. Glob Chang Biol 21:926–934CrossRefPubMedGoogle Scholar
  33. Kuebbing SE, Nuñez MA, Simberloff D (2013) Current mismatch between research and conservation efforts: the need to study co-occurring invasive plant species. Biol Conserv 160:121–129CrossRefGoogle Scholar
  34. Lizarralde MS, Escobar JM (2000) Mamíferos exóticos en la Tierra del Fuego. Ciencia Hoy 10:52–63Google Scholar
  35. Lizarralde MS, Escobar J, Deferrari G (2004) Invader species in Argentina: a review about the beaver (Castor canadensis) population situation on Tierra del Fuego ecosystem. Interciencia 29:532–536Google Scholar
  36. Lockie JD (1961) The food of the pine marten Martes martes in West Ross Shire, Scotland. Proc Zool Soc London 136:187–195CrossRefGoogle Scholar
  37. Macdonald D, Harrington L (2003) The American mink: the triumph and tragedy of adaptation out of context. New Zeal J Zool 30:421–441CrossRefGoogle Scholar
  38. Maley BM, Anderson CB, Stodola K, Rosemond AD (2011) Identifying native and exotic predators of ground-nesting songbirds in Subantarctic forests in Southern Chile. An Inst Patagon 39:51–57CrossRefGoogle Scholar
  39. Martínez Pastur G, Lencinas M, Escobar J et al (2006) Understorey succession in Nothofagus forests in Tierra del Fuego (Argentina) affected by Castor canadensis. Appl Veg Sci 9:143–154CrossRefGoogle Scholar
  40. Moorman M, Eggleston D, Anderson CB, Mansilla A, Szejner P (2009) Implications of beaver Castor canadensis and trout introductions on native fish in the Cape Horn Biosphere Reserve, Chile. Trans Am Fish Soc 138:306–313CrossRefGoogle Scholar
  41. Mott CL, Nielsen CK, Bloomquist CK (2013) Within-lodge interactions between two ecosystem engineers, beavers (Castor canadensis) and muskrats (Ondatra zibethicus). Behaviour 150:1325–1344CrossRefGoogle Scholar
  42. Nuñez MA, Hayward J, Horton TR et al (2013) Exotic mammals disperse exotic fungi that promote invasion by exotic trees. PLoS ONE 8:e66832. doi: 10.1371/journal.pone.0066832 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Pearson OP (1995) Annotated keys for identifying small mammals living in or near Nahuel Huapi National Park or Lanin National Park, Southern Argentina. Mastozoología Neotrop 2:99–148Google Scholar
  44. Previtali A, Cassini MH, Macdonald DW (1998) Habitat use and diet of the American mink (Mustela vison) in Argentinian Patagonia. J Zool 246:482–486CrossRefGoogle Scholar
  45. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Rau J, Martínez DR (2004) Identificación de los órdenes de aves chilenas a través de la microestructura de sus plumas. In: Muñoz A, Rau J, Valenzuela J (eds) Aves rapaces de Chile. CEA Ediciones, ValdiviaGoogle Scholar
  47. Rozzi R, Jiménez JE (2014) Magellanic sub-Antarctic ornithology: first decade of bird studies at the Omora Ethnobotanical Park, Cape Horn Biosphere Reserve, Chile. University of North Texas press, Universidad de Magallanes, Denton, Punta ArenasGoogle Scholar
  48. Rozzi R, Sherriffs MF (2003) El visón (Mustela vison Schreber, Carnivora: Mustelidae), un nuevo mamífero exótico para la Isla Navarino. An Inst Patagon 31:97–104Google Scholar
  49. Rozzi R, Massardo F, Anderson CB, Heidinger K, Silander JA (2006) Ten principles for biocultural conservation at the southern tip of the Americas: the approach of the Omora Ethnobotanical Park. Ecol Soc 11:43–70Google Scholar
  50. Rozzi R, Armesto JJ, Gutiérrez JR et al (2012) Integrating ecology and environmental ethics: earth stewardship in the southern end of the Americas. Bioscience 62:226–236CrossRefGoogle Scholar
  51. Ruscoe WA, Ramsey DSL, Pech RP et al (2011) Unexpected consequences of control: competitive versus predator release in a four-species assemblage of invasive mammals. Ecol Lett 14:1035–1042CrossRefPubMedGoogle Scholar
  52. Schüttler E, Cárcamo J, Rozzi R (2008) Diet of the American mink Mustela vison and its potential impact on the native fauna of Navarino Island, Cape Horn Biosphere Reserve, Chile. Rev Chil Hist Nat 81:585–598CrossRefGoogle Scholar
  53. Schüttler E, Klenke R, McGehee S, Rozzi R, Jax K (2009) Vulnerability of ground-nesting waterbirds to predation by invasive American mink in the Cape Horn Biosphere Reserve, Chile. Biol Conserv 142:1450–1460CrossRefGoogle Scholar
  54. Shier C, Boyce M (2009) Mink prey diversity correlates with mink-muskrat dynamics. J Mammal 90:897–905CrossRefGoogle Scholar
  55. Sielfeld WK, Venegas C, Vanegas CC (1980) Poblamiento e impacto ambiental de Castor canadensis Kuhl, en Isla Navarino, Chile. Anales del Instituto de la Patagonia 11:247–257Google Scholar
  56. Silva C, Saavedra B (2008) Knowing for controlling: ecological effects of invasive vertebrates in Tierra del Fuego. Rev Chil Hist Nat 81:123–136CrossRefGoogle Scholar
  57. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919CrossRefPubMedGoogle Scholar
  58. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  59. Soto GE, Vergara PM, Lizama ME et al (2012) Do beavers improve the habitat quality for magellanic woodpeckers? Bosque 33:271–274CrossRefGoogle Scholar
  60. Tella JL, Lambertucci SA, Speziale KL, Hiraldo F (2016) Large-scale impacts of multiple co-occurring invaders on monkey puzzle forest regeneration, native seed predators and their ecological interactions. Glob Ecol Conserv 6:1–15CrossRefGoogle Scholar
  61. Ulloa E, Anderson CB, Ardón M, Murcia S, Valenzuela AEJ (2012) Organic matter characterization and decomposition dynamics in sub Antarctic streams impacted by invasive beavers. Lat Am J Aquat Res 40:881–892CrossRefGoogle Scholar
  62. Valenzuela AEJ, Raya Rey A, Fasola L et al (2013) Trophic ecology of a top predator colonizing the southern extreme of South America: feeding habits of invasive American mink (Neovison vison) in Tierra del Fuego. Mamm Biol 78:104–110Google Scholar
  63. Valenzuela AEJ, Anderson CB, Fasola L, Cabello JL (2014) Linking invasive exotic vertebrates and their ecosystem impacts in Tierra del Fuego to test theory and determine action. Acta Oecol 54:110–118CrossRefGoogle Scholar
  64. Viljugrein H, Lingjærde OC, Stenseth NC, Boyce MS (2001) Spatio-temporal patterns of mink and muskrat in Canada during a quarter century. J Anim Ecol 70:671–682CrossRefGoogle Scholar
  65. Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol 16:454–459CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Ramiro D. Crego
    • 1
    • 3
    • 5
    Email author
  • Jaime E. Jiménez
    • 1
    • 2
    • 3
    • 4
    • 5
  • Ricardo Rozzi
    • 1
    • 2
    • 3
    • 4
    • 5
  1. 1.Department of Biological SciencesUniversity of North TexasDentonUSA
  2. 2.Department of Philosophy and ReligionUniversity of North TexasDentonUSA
  3. 3.Instituto de Ecología and Biodiversidad, Departamento de Ciencias EcológicasFacultad de CienciasSantiagoChile
  4. 4.Universidad de MagallanesPunta ArenasChile
  5. 5.Sub-Antarctic Biocultural Conservation ProgramUniversity of North TexasDentonUSA

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