Biological Invasions

, Volume 16, Issue 5, pp 1185–1196 | Cite as

Rodent seed predation as a biotic filter influencing exotic plant abundance and distribution

  • D. E. Pearson
  • J. L. Hierro
  • M. Chiuffo
  • D. Villarreal
Original Paper


Biotic resistance is commonly invoked to explain why many exotic plants fail to thrive in introduced ranges, but the role of seed predation as an invasion filter is understudied. Abiotic conditions may also influence plant populations and can interact with consumers to determine plant distributions, but how these factors jointly influence invasions is poorly understood. In central Argentina’s Caldenal savannas, we experimentally examined how seed predation and water availability influenced recruitment/establishment of nine exotic plant invaders over 2 years. We then explored how seed predation patterns related to invasion patterns. Excluding rodent seed predators dramatically increased seedling recruitment for eight of nine exotic species (by 100–300 % in most cases) and increased young/adult plant abundance for four species in one or both years. Adding water to ameliorate drought tended to increase seedling numbers for most species, but these trends were not significant. Vegetation surveys revealed that exotic plant richness was 50 % lower in matrix habitat compared with disturbed roadsides and that cover of the two most aggressive invaders, which were both strongly suppressed by seed predation, was 75–80 % lower in matrix than roadside habitats. Seed offerings indicated seed removal by rodents was 11 times greater in intact matrix habitat compared with roadsides. Rodent seed predation represents a significant source of biotic resistance to plant invasions. Ubiquitous disturbances such as road construction can disrupt this filter. The widely recognized role that disturbance plays in facilitating invasions, which is largely attributed solely to reduced plant competition, may also arise from disruption of top–down controls.


Biotic resistance Road disturbance Plant recruitment Seed predation Water addition 



We thank B. Connolly, A. Litt, Y. Ortega, and anonymous reviewers for valuable feedback on draft manuscripts. L. S. Baggett consulted on statistical analyses. We are in debt to R. Lecitra, F. Miguel, N. Icasatti, and M. Cock for field assistance, and personnel at the Parque Luro Provincial Reserve for logistical support. Rainfall information for Santa Rosa was provided by G. Vergara (Agronomy Department, UNLPam). This project was funded by the President’s Early Career Award in Science and Engineering to D.E.P. and CONICET, ANPCyT, and UNLPam to J.L.H.


  1. Alba-Lynn C, Henk S (2010) Potential for ants and vertebrate predators to shape seed-dispersal dynamics of the invasive thistles Cirsium arvense and Carduus nutans in their introduced range (North America). Plant Ecol 210:291–301CrossRefGoogle Scholar
  2. Allington GRH et al (2013) Niche opportunities and invasion dynamics in a desert annual community. Ecol Lett 16:158–166PubMedCrossRefGoogle Scholar
  3. Bartholomew B (1970) Bare zones between California shrub and grassland communities: the role of animals. Science 170:1210–1212PubMedCrossRefGoogle Scholar
  4. Blaney CS, Kotanen PM (2001) Post-dispersal losses to seed predators: an experimental comparison of native and exotic old field plants. Can J Bot 79:284–292Google Scholar
  5. Brown JH, Heske EJ (1990) Control of a desert–grassland transition by a keystone rodent guild. Science 250:1705–1707PubMedCrossRefGoogle Scholar
  6. Brown JH, Lieberman GA (1973) Resource utilization and coexistence of see-eating desert rodents in sand dune habitats. Ecology 54:788–797CrossRefGoogle Scholar
  7. Cano E (1980) Inventario integrado de los recursos naturales de la provincia de La Pampa. INTA-UNLPam, Buenos Aires, Argentina (In Spanish)Google Scholar
  8. Carrillo-Gavilán MA et al (2010) Comparing seed removal of 16 pine species differing in invasiveness. Biol Invasions 12:2233–2242CrossRefGoogle Scholar
  9. Carrillo-Gavilán MA et al (2012) Establishment constraints of an alien and a native conifer in different habitats. Biol Invasions 14:1279–1289CrossRefGoogle Scholar
  10. Chiuffo M (2009) Efecto de las picadas y caminos en la invasion de especies herbaceas en la reserva provincial Parque Luro. Undergraduate’s Thesis, Universidad Nacional de La Pampa, Santa Rosa, ArgentinaGoogle Scholar
  11. Cushman JH et al (2011) Native herbivores and plant facilitation mediate the performance and distribution of an invasive exotic grass. J Ecol 99:524–531Google Scholar
  12. Davis MA et al (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  13. DeWalt SJ et al (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecol 85:471–483Google Scholar
  14. Eckberg JO et al (2012) Insect herbivory and propagules pressure influence Cirsium vulgare invasiveness across the landscape. Ecology 93:1787–1794PubMedCrossRefGoogle Scholar
  15. Edwards GR, Crawley MJ (1999) Rodent seed predation and seedling recruitment in mesic grassland. Oecologia 118:288–296CrossRefGoogle Scholar
  16. Ellis BA et al (1998) Dietary habits of the common rodents in an agroecosystem in Argentina. J Mammal 79:1203–1220CrossRefGoogle Scholar
  17. Elton C (1958) The ecology of invasions by animals and plants. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  18. Eriksson O, Ehrlen J (1992) Seed and microsite limitation of recruitment in plant populations. Oecologia 91:360–364CrossRefGoogle Scholar
  19. Ferreira AV et al (2011) Seed predators limit plant recruitment in Neotropical savannas. Oikos 120:1013–1022CrossRefGoogle Scholar
  20. Gelbard JL, Belnap J (2003) Roads as conduits for exotic plant invasions in a semiarid landscape. Conserv Biol 17:420–432CrossRefGoogle Scholar
  21. Giannoni SM et al (2005) Main food categories in diets of sigmodontine rodents in the Monte (Argentina). Mast Neotrop 12:181–187Google Scholar
  22. Hierro JL et al (2009) Germination responses of an invasive species in native and non-native ranges. Oikos 118:529–538CrossRefGoogle Scholar
  23. Hierro JL et al (2011) Resistance to Centaurea solstitiatis invasion from annual and perennial grasses in California and Argentina. Biol Invasions 13:2249–2259CrossRefGoogle Scholar
  24. Inouye RS et al (1980) Effects of predation and competition on survivorship, fecundity, and community structure of desert annuals. Ecology 61:1344–1351CrossRefGoogle Scholar
  25. Kelt DA et al (1984) Seed predation by birds and small mammals in semiarid Chile. Oikos 104:133–141CrossRefGoogle Scholar
  26. Lambrinos JG (2006) Spatially variable propagule pressure and herbivory influence invasion of chaparral shrubland by an exotic grass. Oecologia 147:327–334PubMedCrossRefGoogle Scholar
  27. Levine JM et al (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  28. Louda SM (1982) Variation in plant recruitment over a gradient in relation to insect seed predation. Ecol Monogr 52:25–41CrossRefGoogle Scholar
  29. Louda SM (1983) Seed predation and seedling mortality in the recruitment of a shrub, Haplopappus venetus (Aseraceae), along a climatic gradient. Ecology 64:511–521CrossRefGoogle Scholar
  30. Louda SM, Rodman JE (1996) Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, Bittercress). J Ecol 84:229–237CrossRefGoogle Scholar
  31. Mack RN (1996) Biotic barriers to plant naturalization. In: Moran VC, Hoffmann JH (eds) Proceedings of the IX international symposium on biological control of weeds. University of Cape Town Stellenbosch, South Africa, pp 39–46Google Scholar
  32. Mares MA, Rosenzweig ML (1978) Granivory and North and South American deserts: rodents, birds, and ants. Ecology 59:235–241CrossRefGoogle Scholar
  33. Maron JL, Crone EC (2006) Herbivory: effects on plant abundance, distribution, and population growth. Proc R Soc B 273:2575–2584Google Scholar
  34. Maron JL, Kauffman MJ (2006) Habitat-specific impacts of multiple consumers on plant population dynamics. Ecology 87:113–124PubMedCrossRefGoogle Scholar
  35. Maron JL, Simms EL (2001) Rodent-limited establishment of bush lupine: field experiments on the cumulative effect of granivory. J Ecol 89:578–588CrossRefGoogle Scholar
  36. Maron JL et al (2012) Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100:1492–1500CrossRefGoogle Scholar
  37. Mills JN et al (1992) Reproductive characteristics of rodent assemblages in cultivated regions of central Argentina. J Mammal 73:515–526CrossRefGoogle Scholar
  38. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627PubMedCrossRefGoogle Scholar
  39. Mittelbach GG, Gross KL (1984) Experimental studies of seed predation in old-fields. Oecologia 65:7–13CrossRefGoogle Scholar
  40. Nuñez MA et al (2008) Seed predation as a barrier to alien conifer invasions. Biol Invasions 10:1389–1398CrossRefGoogle Scholar
  41. Orrock JL et al (2006) See predation, not seed dispersal, explains the landscape-level abundance of an early-successional plant. J Ecol 94:838–845CrossRefGoogle Scholar
  42. Orrock JL et al (2008) Apparent competition with an exotic plant reduces native plant establishment. Ecology 89:1168–1174PubMedCrossRefGoogle Scholar
  43. Ortega YK et al (2012) Population-level compensation impedes biological control of an invasive forb and indirect release of a native grass. Ecology 93:783–792PubMedCrossRefGoogle Scholar
  44. Ostfeld RS et al (1997) Effects of rodents on survival of tree seeds and seedlings in invading old fields. Ecology 78:1531–1542CrossRefGoogle Scholar
  45. Parker JD et al (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461PubMedCrossRefGoogle Scholar
  46. Pearson DE, Callaway RM (2008) Weed biocontrol insects reduce native plant recruitment through second-order apparent competition. Ecol Appl 18:1489–1500PubMedCrossRefGoogle Scholar
  47. Pearson DE, Fletcher RJ Jr (2008) Mitigating exotic impacts: restoring native deer mouse populations elevated by an exotic food subsidy. Ecol Appl 18:321–334PubMedCrossRefGoogle Scholar
  48. Pearson DE et al (2011) Biotic resistance via granivory: establishment by invasive, naturalized and native asters reflects generalist preference. Ecology 92:1748–1757PubMedCrossRefGoogle Scholar
  49. Pearson DE et al (2012) Biotic resistance: exclusion of native rodent consumers releases populations of a weak invader. J Ecol 100:1383–1390CrossRefGoogle Scholar
  50. Pierson EA, Mack RN (1990) The population biology of Bromus tectorum in forests: distinguishing the opportunity for dispersal from environmental restriction. Oecologia 84:519–525Google Scholar
  51. Reader RJ (1993) Control of seedling emergence by ground cover and seed predation in relation to seed size for some old-field species. J Ecol 81:169–175CrossRefGoogle Scholar
  52. SAS Institute (2009) SAS/STAT User’s Guide, Version 9.2. SAS Institute Inc., CaryGoogle Scholar
  53. Shahid A et al (2009) Selection of seeds of common native and non-native plants by granivorous rodents in the northeastern United States. Am Mid Nat 162:207–212CrossRefGoogle Scholar
  54. Shea K et al (2005) Context-dependent biological control of an invasive thistle. Ecol 86:3174–3181Google Scholar
  55. Smith SE et al (2000) Geographic variation in predictive seedling emergence in a perennial desert grass. J Ecol 88:139–149CrossRefGoogle Scholar
  56. Troiani H, Steibel P (2008) Reconocimiento de malezas: Región subhúmeda y semiárida pampeana. Universidad Nacional de La Pampa, Colegio de Ingenieros Agrónomos de La Pampa, Santa Rosa (In Spanish)Google Scholar
  57. Vilá M, Gimeno I (2003) Seed predation of two alien Opuntia species invading Mediterranean communities. Plant Ecol 167:1–8CrossRefGoogle Scholar
  58. Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170CrossRefGoogle Scholar
  59. Yahnke CJ et al (2001) Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan Chaco. Am J Trop Med Hyg 65:768–776PubMedGoogle Scholar
  60. Zwolak R et al (2010) Fire and mice: seed predation moderates fire’s influence on conifer recruitment. Ecology 91:1124–1131PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2013

Authors and Affiliations

  • D. E. Pearson
    • 1
    • 2
  • J. L. Hierro
    • 3
    • 4
  • M. Chiuffo
    • 3
  • D. Villarreal
    • 4
  1. 1.Rocky Mountain Research StationU.S.D.A. Forest ServiceMissoulaUSA
  2. 2.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  3. 3.INCITAP (CONICET-UNLPam)Santa RosaArgentina
  4. 4.Facultad de Ciencias Exactas y NaturalesUniversidad Nacional de La PampaSanta RosaArgentina

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