Biological Invasions

, Volume 20, Issue 3, pp 583–591 | Cite as

Ungulates can control tree invasions: experimental evidence from nonnative conifers and sheep herbivory

  • L. B. Zamora Nasca
  • M. A. Relva
  • M. A. Núñez
Original Paper


Invasive conifer species are increasingly recognized as a serious problem in many parts of the world, where they are having large ecological and economic impacts. Understanding factors that trigger and can control invasion is key to management. Grazing and browsing by large herbivores have been suggested as a mechanism that may halt conifer invasions, although conflicting results have been reported (i.e. positive, negative or no effect of grazing on invasion). We believe that some of these opposing responses arise due to the absence of well-planned and replicated experiments, since current evidence is mostly observational, and for example, differences in animal densities can produce different results. Thus, in this study, we tested whether large herbivores can control invasion by nonnative conifers and whether the severity of the invasion process would be lessened by increased herbivory intensity. We evaluate experimentally herbivore damage on Pinus contorta, a highly invasive species in many countries of the Southern Hemisphere, under different sheep stocking rates in Patagonia, Argentina. We used four stocking rates, corresponding to 1, 2, 4 and 8 times the recommended sheep herbivory intensity for the study area. The response was not linear but rather presented a threshold. The greater stocking rate, the greater the browsing, higher reduction in seedling height, and decrease of survival of P. contorta. Also, the highest stocking rate damaged and killed 99% of them. This study provides evidence that large domestic herbivores can play a key role in the invasion process and, if managed properly, would provide a tool to help limit conifer invasion.


Biological invasion Browsing Large mammalian herbivore Pinus contorta Sheep Steppe 



We are grateful to The Nature Conservancy and Fortin Chacabuco ranch for helping and allowing us to work in the area and to the technician Pablo Alvear for his help in field job. We thank D. Simberloff, E. Chaneton, L. Montti and two anonymous reviewers for valuable comments on earlier drafts that greatly improved the manuscript. This work was supported with a grant from “Agencia Nacional de Promoción Científica y Tecnológica” of Argentina (PICT 2012-2283).

Supplementary material

10530_2017_1558_MOESM1_ESM.pdf (137 kb)
Online resource 1 Experimental design (PDF 137 kb)
10530_2017_1558_MOESM2_ESM.pdf (353 kb)
Online resource 2 Details of data analysis (PDF 353 kb)
10530_2017_1558_MOESM3_ESM.pdf (138 kb)
Online resource 3 Details of the results of the hierarchical Bayesian models. (PDF 137 kb)


  1. Bailey DW (2004) Management strategies for optimal grazing distribution and use of arid rangelands. J Anim Sci 82:E147–E153. doi: 10.2527/2004.8213_supplE147x PubMedGoogle Scholar
  2. Bava JO, Loguercio GA, Salvador G (2015) ¿Por qué plantar en Patagonia? Estado actual y el rol futuro de los bosques plantados. Ecol Austral 25:101–111Google Scholar
  3. Becerra PI, Bustamante RO (2009) The effect of herbivory on seedling survival of the invasive exotic species Pinus radiata and Eucalyptus globulus in a Mediterranean ecosystem of Central Chile. For Ecol Manag 256:1573–1578. doi: 10.1016/j.foreco.2008.04.011 CrossRefGoogle Scholar
  4. Bonvissuto GL, Somlo RC, Lanciotti ML et al (2008) Guías de Condición para Pastizales Naturales de “Precordillera”, “Sierras y Mesetas” y “Monte Austral” de Patagonia. Instituto Nacional de Tecnología Agrpecuaria - INTA, Buenos AiresGoogle Scholar
  5. Borrelli P, Boggio F, Sturzenbaum P et al (2013) Grassland regeneration and sustainability standard (GRASS). The Nature Conservancy - Ovis XXI S.A., Buenos AiresGoogle Scholar
  6. Boulant N, Kunstler G, Rambal S, Lepart J (2008) Seed supply, drought, and grazing determine spatio-temporal patterns of recruitment for native and introduced invasive pines in grasslands. Divers Distrib 14:862–874. doi: 10.1111/j.1472-4642.2008.00494.x CrossRefGoogle Scholar
  7. Bran D, Ayesa J, Lopez C (2002) Áreas ecológicas de Neuquen. Instituto Nacional de Tecnología Agropecuaria - INTA, BarilocheGoogle Scholar
  8. Briske DD, Bestelmeyer BT, Brown JR et al (2013) The Savory method can not green deserts or reverse climate change. Rangelands 35:72–74. doi: 10.2111/RANGELANDS-D-13-00044.1 CrossRefGoogle Scholar
  9. Butterfield J, Bingham S, Savory A (2006) Holistic management handbook: healthy land, healthy profits. Island Press, WashingtonGoogle Scholar
  10. Cibils AF, Lira Fernández RJ, Oliva GE, Escobar JM (2014) Is holistic management really saving patagonian rangelands from degradation? A response to Teague. Rangelands 36:26–27. doi: 10.2111/Rangelands-D-14-00011.1 CrossRefGoogle Scholar
  11. Crozier ER, Ledgard NJ (1990) Palatability of wilding conifers and control by simulated sheep browsing. In: Basset C, Whitehouse LJ, Zabkiewicz JA (eds) Alternatives to the chemical control of weeds. Proceedings of international conference, Rotorua, July 1989. Bulletin No 155. Ministry of Forestry, Forest Research Institute, Christchurch, New Zealand, pp 139–143Google Scholar
  12. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211. doi: 10.1146/132403 CrossRefGoogle Scholar
  13. de Villalobos AE, Zalba SM, Peláez DV (2011) Pinus halepensis invasion in mountain pampean grassland: effects of feral horses grazing on seedling establishment. Environ Res 111:953–959. doi: 10.1016/j.envres.2011.03.011 CrossRefPubMedGoogle Scholar
  14. di Virgilio A, Morales JM (2016) Towards evenly distributed grazing patterns: including social context in sheep management strategies. PeerJ 4:e2152. doi: 10.7717/peerj.2152 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Easdale MH, Aguiar MR, Roman M, Villagra S (2009) Comparación socio-económica de dos regiones biofísicas: los sistemas ganaderos de la provincia de Río Negro, Argentina. Cuad Desarro Rural 6:173–198Google Scholar
  16. Edenius L, Danell K, Bergström R (1993) Impact of herbivory and competition on compensatory growth in woody plants: winter browsing by moose on Scots pine. Oikos 66:286–292CrossRefGoogle Scholar
  17. Eschtruth AK, Battles JJ (2008) Deer herbivory alters forest response to canopy decline caused by an exotic insect pest. Ecol Appl 18:360–376. doi: 10.1890/07-0446.1 CrossRefPubMedGoogle Scholar
  18. Gelman A, Hill J (2007) Why? In: Gelman A, Hill J (eds) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge, pp 1–11Google Scholar
  19. Gundale MJ, Pauchard A, Langdon B et al (2014) Can model species be used to advance the field of invasion ecology? Biol Invasions 16:591–607. doi: 10.1007/s10530-013-0610-0 CrossRefGoogle Scholar
  20. Hester A, Bergman M, Iason G, Moen J (2006) Impacts of large herbivores on plant community structure and dynamics. In: Danell K, Bergström R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamic and conservation. Cambridge University Press, Cambridge, p 506Google Scholar
  21. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15. doi: 10.1111/j.1365-2745.2004.00953.x CrossRefGoogle Scholar
  22. Hobbs RJ (2001) Synergisms among habitat fragmentation, livestock grazing, and biotic invasions in Southwestern Australia. Conserv Biol 15:1522–1528CrossRefGoogle Scholar
  23. Hobbs NT (2006) Large herbivores as sources of disturbances in ecosystems. In: Danell K, Bergström R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation. Cambridge University Press, Cambridge, pp 261–288CrossRefGoogle Scholar
  24. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Ecosyst Manag 6:324–337Google Scholar
  25. Knight TM, Dunn JL, Smith LA et al (2009) Deer facilitate invasive plant succes in a Pennsylvania forest understory. Nat Areas J 29:110–116CrossRefGoogle Scholar
  26. Kurtz DB, Asch F, Giese M et al (2016) High impact grazing as a management tool to optimize biomass growth in northern Argentinean grassland. Ecol Indic 63:100–109. doi: 10.1016/j.ecolind.2015.10.065 CrossRefGoogle Scholar
  27. Lalampaa PK, Wasonga OV, Rubenstein DI, Njoka JT (2016) Effects of holistic grazing management on milk production, weight gain, and visitation to grazing areas by livestock and wildlife in Laikipia County, Kenya. Ecol Process 5:17. doi: 10.1186/s13717-016-0061-5 CrossRefGoogle Scholar
  28. Lamarque LJ, Delzon S, Lortie CJ (2011) Tree invasions: a comparative test of the dominant hypotheses and functional traits. Biol Invasions 13:1969–1989. doi: 10.1007/s10530-011-0015-x CrossRefGoogle Scholar
  29. Langdon B, Pauchard A, Aguayo M (2010) Pinus contorta invasion in the Chilean Patagonia: local patterns in a global context. Biol Invasions 12:3961–3971. doi: 10.1007/s10530-010-9817-5 CrossRefGoogle Scholar
  30. Ledgard NJ, Norton DA (2008) The impact of browsing on wilding conifers in the South Island high country. N Z J For 52:29–34Google Scholar
  31. Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Wiley, UKGoogle Scholar
  32. Lonsdale WM (1999) Global patterns of plants invasions and the concept of invasibility. Ecology 80:1522–1536CrossRefGoogle Scholar
  33. Loydi A, Zalba SM (2009) Feral horses dung piles as potential invasion windows for alien plant species in natural grasslands. Plant Ecol 201:471–480. doi: 10.1007/978-90-481-2798-6_9 CrossRefGoogle Scholar
  34. Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  35. McGregor KF, Watt MS, Hulme PE, Duncan RP (2012) What determines pine naturalization: species traits, climate suitability or forestry use? Divers Distrib 18:1013–1023. doi: 10.1111/j.1472-4642.2012.00942.x CrossRefGoogle Scholar
  36. Moreira X, Mooney KA, Rasmann S et al (2014) Trade-offs between constitutive and induced defences drive geographical and climatic clines in pine chemical defences. Ecol Lett 17:537–546. doi: 10.1111/ele.12253 CrossRefPubMedGoogle Scholar
  37. Nuñez MA, Medley KA (2011) Pine invasions: climate predicts invasion success; something else predicts failure. Divers Distrib 17:703–713. doi: 10.1111/j.1472-4642.2011.00772.x CrossRefGoogle Scholar
  38. Nuñez MA, Chiuffo M, Torres A et al (in press) Ecology and management of invasive Pinaceae around the world: progress and challenges. Biol Invasions. doi:  10.1007/s10530-017-1483-4
  39. Nuñez MA, Moretti A, Simberloff D (2011) Propagule pressure hypothesis not supported by an 80-year experiment on woody species invasion. Oikos 120:1311–1316. doi: 10.1111/j.1600-0706.2011.19504.x CrossRefGoogle Scholar
  40. Nuñez MA, Hayward J, Horton TR et al (2013) Exotic mammals disperse exotic fungi that promote invasion by exotic trees. PLoS ONE 8:1–6. doi: 10.1371/journal.pone.0066832 CrossRefGoogle Scholar
  41. Odadi WO, Fargione J, Rubenstein DI (2017) Vegetation, wildlife and livestock responses to planned grazing management in an african pastoral landscape. L Degrad Dev. doi: 10.1002/ldr.2725 Google Scholar
  42. Oduor AMO, Gómez JM, Strauss SY (2010) Exotic vertebrate and invertebrate herbivores differ in their impacts on native and exotic plants: a meta-analysis. Biol Invasions 12:407–419. doi: 10.1007/s10530-009-9622-1 CrossRefGoogle Scholar
  43. Oliva G, Ferrante D, Puig S, Williams M (2012) Sustainable sheep management using continuous grazing and variable stocking rates in Patagonia: a case study. Rangel J 34:285–295. doi: 10.1071/RJ12016 CrossRefGoogle Scholar
  44. Osem Y, Lavi A, Rosenfeld A (2011) Colonization of Pinus halepensis in Mediterranean habitats: consequences of afforestation, grazing and fire. Biol Invasions 13:485–498. doi: 10.1007/s10530-010-9843-3 CrossRefGoogle Scholar
  45. Paramidani M, Doffigny C, Codesal P (2014) Estudio inicial de Pastizales Ea. “Fortín Chacabuco”. Ovis XXI S.A., Buenos Aires, p 28Google Scholar
  46. Parker J, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967. doi: 10.1111/j.1461-0248.2005.00799.x CrossRefGoogle Scholar
  47. Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Hornik K, Leisch F, Zeileis A (eds) Proceedings of the 3rd international workshop on distributed statistical computing. pp 1–10Google Scholar
  48. Porath ML, Momont PA, DelCurto T et al (2002) Offstream water and trace mineral salt as management strategies for improved cattle distribution. J Anim Sci 80:346–356. doi: 10.2527/2002.802346x CrossRefPubMedGoogle Scholar
  49. R Development Core Team (2015) R: a language and environment for statistical computing. R Development Core Team, ViennaGoogle Scholar
  50. Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661CrossRefGoogle Scholar
  51. Relva MA, Nuñez MA, Simberloff D (2010) Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Invasions 12:303–311. doi: 10.1007/s10530-009-9623-0 CrossRefGoogle Scholar
  52. Richardson DM (2006) Pinus: a model group for unlocking the secrets of alien plant invasions? Preslia 78:375–388Google Scholar
  53. Richardson DM, Bond WJ (1991) Determinants of plant distribution: evidence from pine invasions stable. Am Nat 137:639–668CrossRefGoogle Scholar
  54. Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr 30:409–431CrossRefGoogle Scholar
  55. Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809. doi: 10.1111/j.1472-4642.2011.00782.x CrossRefGoogle Scholar
  56. Richardson DM, Wilgen BW, Nuñez MA (2007) Alien conifer invasions in South America: short fuse burning? Biol Invasions 10:573–577. doi: 10.1007/s10530-007-9140-y CrossRefGoogle Scholar
  57. Richardson DM, Williamst PA, Hobbs RJ (2011) Pine invasions in the Southern Hemisphere: determinants of spread and invadability. J Biogeogr 21:511–527CrossRefGoogle Scholar
  58. Rundel PW, Dickie IA, Richardson DM (2014) Tree invasions into treeless areas: mechanisms and ecosystem processes. Biol Invasions 16:663–675. doi: 10.1007/s10530-013-0614-9 CrossRefGoogle Scholar
  59. Sarasola MM, Rusch V, Schlichter TM, Ghersa CM (2006) Invasión de coníferas forestales en áreas de estepa y bosques de ciprés de la cordillera en la Región Andino Patagónica. Ecol Austral 16:143–156Google Scholar
  60. Savory A (1983) The Savory grazing method or holistic resource management. Rangelands 5:155–159Google Scholar
  61. Schlichter TM, Laclau P (1998) Ecotono estepa-bosque y plantaciones forestales en la Patagonia norte. Ecol Austral 8:285–296Google Scholar
  62. Siffredi GL, Boggio F, Giorgetti H et al (2013) Guía para la evaluación de Pastizales. Para las áreas ecológicas de Sierras y Mesetas Occidentales y de Monte de Patagonia Norte. INTA, BarilocheGoogle Scholar
  63. Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268. doi: 10.1007/s10530-011-9956-3 CrossRefGoogle Scholar
  64. Simberloff D, Relva MA, Nuñez MA (2002) Gringos en el bosque: introduced tree invasion in a native Nothofagus/Austrocedrus forest. Biol Invasions 4:35–53CrossRefGoogle Scholar
  65. Simberloff D, Nuñez MA, Ledgard NJ et al (2010) Spread and impact of introduced conifers in South America: lessons from other southern hemisphere regions. Austral Ecol 35:489–504. doi: 10.1111/j.1442-9993.2009.02058.x CrossRefGoogle Scholar
  66. Six L, Bakker J, Bilby R (2013) Loblolly pine germination and establishment in plantations and grasslands of northern Uruguay. For Ecol Manage 302:1–6CrossRefGoogle Scholar
  67. Spear D, Chown SL (2009) Non-indigenous ungulates as a threat to biodiversity. J Zool 279:1–17CrossRefGoogle Scholar
  68. Squibb RC, Provenza FD, Balph DF (1990) Effect of age of exposure on consumption of a shrub by sheep. J Anim Sci 68:987–997CrossRefPubMedGoogle Scholar
  69. Teague R (2014) Deficiencies in the Briske et al. Rebuttal of the savory method. Rangelands 36:37–38. doi: 10.2111/1551-501X-36.1.37 CrossRefGoogle Scholar
  70. TNC (2016) Estancia demostrativa Fortín Chacabuco—Lineamientos de Manejo. The Nature Conservancy, San Carlos de Bariloche, p 43Google Scholar
  71. Vavra M, Parks CG, Wisdom MJ (2007) Biodiversity, exotic plant species, and herbivory: the good, the bad, and the ungulate. For Ecol Manag 246:66–72. doi: 10.1016/j.foreco.2007.03.051 CrossRefGoogle Scholar
  72. Walker JW, Hemenway KG, Hatfield PG, Glimp HA (1992) Training lambs to be weed eaters: studies with leafy spurge. J Range Manag 45:245–249CrossRefGoogle Scholar
  73. Zamora R, Gómez JM, Hódar JA et al (2001) Effect of browsing by ungulates on sapling growth of Scots pine in a mediterranean environment: consequences for forest regeneration. For Ecol Manag 144:33–42. doi: 10.1016/S0378-1127(00)00362-5 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Instituto de Investigaciones en Biodiversidad y Medio AmbienteCONICET- Universidad Nacional del ComahueBarilocheArgentina
  2. 2.Grupo de Ecología de InvasionesINIBIOMA, CONICET, Universidad Nacional del ComahueBarilocheArgentina

Personalised recommendations