pp 1–11 | Cite as

Seed predation does not explain pine invasion success

  • Jaime MoyanoEmail author
  • Mariana C. Chiuffo
  • Martín A. Nuñez
  • Mariano A. Rodriguez-Cabal
Plant-microbe-animal interactions – original research


Why some non-native plant species invade, and others fail remains an elusive question. Plant invasion success has been associated with specific species traits. Yet, we have limited knowledge of the mechanisms relating these traits to invasion potential. General patterns of biotic resistance by seed predation may provide a mechanism that helps separate invasive from non-invasive plants. Seed predation is an important barrier against plant establishment for many plant species. It may, therefore, create a selective filter against non-native plant establishment based on plant traits related to seed predation rate. In two cafeteria-style seed predation experiments in a steppe ecosystem in Patagonia (Argentina) we provided seeds of 16 non-native Pinaceae covering a 300-fold variation in seed mass, a 200-fold variation in seed volume and 75-fold variation in seed toughness. Seed removal decreased with seed mass and seed volume. Seed toughness was not a significant predictor while seed volume was the best predictor of predators’ preference. However, for species of this family small seed size is the most important predictor of species invasiveness. Our results show that seed predation does not explain Pinaceae invasive success. In our system, species that have smaller seeds (i.e., more invasive) are preferentially consumed by seed predators. Seed mass was not the best predictor of granivory rates, despite being the seed trait on which most studies have been focused. Our ability to predict future invasion and understand invasion success could benefit from other studies that focus on the mechanisms behind invasive traits.


Biotic resistance Invasive plants Invasive traits Pinus Seed traits 



This research was supported by Rufford Foundation Grant number 23089-1 and the National Agency of Scientific and Technologic Promotion (AGENCIA) grant “PICT 2014 No 0662 PRESTAMO BID”. We thank San Ramon ranch for their help in this study. We also thank Ariel Mayoral and Josefina Uijt den Bogaard for their valuable help on the field. We are very grateful with René Rodriguez, Alejandro Yawny and Graciela Bertolino from the National Centre of Atomic Energy (CNEA) for help with measurements of seed toughness and providing us access to their Instron 5567 Universal Testing Machine. We appreciate the help with the statistical analyzes provided by Florencia Tiribelli. Mauro Tammone helped with the identification of small mammals. We greatly appreciate the helpful comments from Adam Davis and Rob Gibson on an earlier version of this manuscript.

Author contribution statement

JM, MC, MN, and MRC conceived the idea and JM designed the methodology with help from all the authors. JM carried out the experiments and collected the data with help from MC. All authors participated in the discussion of the results. JM led the writing of the manuscript. MC, MN, and MRC revised the manuscript and made comments to improve it. All authors gave final approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2019_4354_MOESM1_ESM.docx (96 kb)
Supplementary file1 (DOCX 96 kb)


  1. Abbott HG (1962) Tree seed preferences of mice and voles in the northeast. J Forest 60:97–99. CrossRefGoogle Scholar
  2. Amin MN, Hossain MA, Roy KC (2004) Effects of moisture content on some physical properties of lentil seeds. J Food Eng 65:83–87. CrossRefGoogle Scholar
  3. Anandu P, Sangeetha K, Sanjana P, Santhosh R, Mahendran R (2018) Physical properties of infrared (IR) assisted hot air dried nutmeg (Myristica fragrans) seeds. J Food Process Preserv 42:e13359. CrossRefGoogle Scholar
  4. Anchorena J, Cingolani A (2002) Identifying habitat types in a disturbed area of the forest-steppe ecotone of Patagonia. Plant Ecol 158:97–112CrossRefGoogle Scholar
  5. Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. CrossRefGoogle Scholar
  6. Beaujean A (2012) BaylorEdPsych: R package for Baylor University educational psychology quantitative courses. R package version 0.5. R Foundation for Statistical Computing, Vienna, Austria. Available at:
  7. Blate GM, Peart DR, Leighton M (1998) Post-dispersal predation on isolated seeds: a comparative study of 40 tree species in a Southeast Asian rainforest. Oikos 82:522–538. CrossRefGoogle Scholar
  8. Brewer SW (2001) Predation and dispersal of large and small seeds of a tropical palm. Oikos 92:245–255CrossRefGoogle Scholar
  9. Bucyanayandi J-D, Bergeron J-M, Menard H (1990) Preference of meadow voles (Microtus pennsylvanicus) for conifer seedlings: chemical components and nutritional quality of bark of damaged and undamaged trees. J Chem Ecol 16:2569–2579. CrossRefGoogle Scholar
  10. Caley P, Groves RH, Barker R (2008) Estimating the invasion success of introduced plants. Divers Distrib 14:196–203. CrossRefGoogle Scholar
  11. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366. CrossRefGoogle Scholar
  12. CIEFAP (2017) Inventario nacional de plantaciones forestales: Región Patagónica. Ministerio de Agroindustria, ArgentinaGoogle Scholar
  13. Connolly B, Pearson D, Mack R (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95:1759–1769CrossRefGoogle Scholar
  14. Crawley MJ (1997) Plant–herbivore dynamics. In: Crawley MJ (ed) Plant ecology. Blackwell Scientific Publications, Oxford, pp 401–474Google Scholar
  15. Crawley MJ (2000) Crawley MJ (2000) Seed predators and plant population dynamics. In: Gallagher RS (ed) Seeds: the ecology of regeneration in plant communities. CABI International, Wallingford, pp 167–182CrossRefGoogle Scholar
  16. Di Pierro E et al (2011) The effects of seed availability on habitat use by a specialist seed predator. Eur J Wildl Res 57:585–595. CrossRefGoogle Scholar
  17. Dutta SK, Nema VK, Bhardwaj RK (1988) Physical properties of gram. J Agric Eng Res 39:259–268. CrossRefGoogle Scholar
  18. Emerson SE, Brown JS, Whelan CJ, Schmidt KA (2012) Scale-dependent neighborhood effects: shared doom and associational refuge. Oecologia 168:659–670. CrossRefGoogle Scholar
  19. Essl F, Moser D, Dullinger S, Mang T, Hulme P (2010) Selection for commercial forestry determines global patterns of alien conifer invasions. Biodivers Res 16:911–921. Google Scholar
  20. Essl F, Mang T, Dullinger S, Moser D, Hulme PE (2011) Macroecological drivers of alien conifer naturalizations worldwide. Ecography 34:1076–1084. CrossRefGoogle Scholar
  21. Franzese J, Raffaele E (2017) Fire as a driver of pine invasions in the Southern Hemisphere: a review. Biol Invasions 19:2237–2246. CrossRefGoogle Scholar
  22. Fricke EC, Wright SJ (2016) The mechanical defence advantage of small seeds. Ecol Lett 19:987–991. CrossRefGoogle Scholar
  23. Garren JM, Strauss SY (2009) Population-level compensation by an invasive thistle thwarts biological control from seed predators. Ecol Appl 19:709–721CrossRefGoogle Scholar
  24. Gómez JM (2004) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58:71–80. CrossRefGoogle Scholar
  25. Grodzinski W, Sawicka-Kapusta K (1970) Energy values of tree-seeds eaten by small mammals. Oikos 21:52–58. CrossRefGoogle Scholar
  26. Grotkopp E, Rejmánek M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 Pine (Pinus) species. Am Nat 159:396–419. Google Scholar
  27. Grotkopp E, Rejmánek M, Sanderson MJ, Rost TL (2004) Evolution of genome size in pines (Pinus) and its life-history correlates: supertree analyses. Evolution 58(8):1705–1729. CrossRefGoogle Scholar
  28. Hamilton MA et al (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074. CrossRefGoogle Scholar
  29. Hay ME (1986) Associational plant defenses and the maintenance of species diversity: turning competitors into accomplices. Am Nat 128:617–641CrossRefGoogle Scholar
  30. Hjalten J, Danell K, Lundberg P (1993) Herbivore avoidance by association: vole and hare utilization of woody plants. Oikos 68:125–131. CrossRefGoogle Scholar
  31. Hoffmann LA, Redente EF, McEwen LC (1995) Effects of selective seed predation by rodents on shortgrass establishment. Ecol Appl 5:200–208. CrossRefGoogle Scholar
  32. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229. CrossRefGoogle Scholar
  33. Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430CrossRefGoogle Scholar
  34. Hulme PE (1994) Post-dispersal seed predation in grassland: its magnitude and sources of variation. J Ecol 82:645–652. CrossRefGoogle Scholar
  35. Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol Evolut Syst 1:32–46. CrossRefGoogle Scholar
  36. Hulme PE, Borelli T (1999) Variability in post-dispersal seed predation in deciduous woodland: relative importance of location, seed species, burial and density. Plant Ecol 145:149–156. CrossRefGoogle Scholar
  37. Ibrahim MA, Kainulainen P, Aflatuni A, Tiilikkala K, Holopainen JK 2011 Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: With special reference to limenone and its suitability from control of insect pests. J Agric Food10 243 259Google Scholar
  38. James S (2016) James S (2016) An introduction to data analysis using aggregation functions in R. Springer, ChamCrossRefGoogle Scholar
  39. Jansen P, et al. (2002) The role of seed size in dispersal by a scatter-hoarding rodent. In: Levey et al. (ed) Seed dispersal and frugivory: ecology, evolution and conservation. CABI International, Brazil, pp 209–225Google Scholar
  40. Janzen DH (1969) Seed-eaters versus seed size, number, toxicity and dispersal. Evolution 23:1–27. CrossRefGoogle Scholar
  41. Krugman SL, Jenkinson JL (2008) Pinaceae—Pine family. In: Bonner FT, Karraft RP (eds) The woody plant seed manual. Agriculture handbook 727. USDA Forest Service, Washington DC, pp 809–847Google Scholar
  42. Larios L, Pearson DE, Maron JL (2017) Incorporating the effects of generalist seed predators into plant community theory. Funct Ecol 31:1856–1867. CrossRefGoogle Scholar
  43. Leopold AC (1983) Volumetric Components of Seed Imbibition. Plant Physiol 73:677–680. CrossRefGoogle Scholar
  44. Lobo N, Duong M, Millar JS (2009) Conifer-seed preferences of small mammals. Can J Zool 87:773–780. CrossRefGoogle Scholar
  45. Long FL (1934) Application of calorimetric methods to ecological research. Plant Physiol 9:323–337CrossRefGoogle Scholar
  46. Louda SM (1983) Seed predation and seedling mortality in the recruitment of a shrub, Haplopappus venetus (Asteraceae), along a climatic gradient. Ecology 64:511–521CrossRefGoogle Scholar
  47. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609. CrossRefGoogle Scholar
  48. Martell AM (1979) Selection of conifer seeds by deer mice and red-backed voles. Can J For Res 9:201–204. CrossRefGoogle Scholar
  49. 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. CrossRefGoogle Scholar
  50. Moles AT, Warton DI, Westoby M (2003) Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84:3148–3161. CrossRefGoogle Scholar
  51. Moodley D, Geerts S, Richardson DM, Wilson JRU (2013) Different traits determine introduction, naturalization and invasion success in woody plants: proteaceae as a test case. PLoS One 8:e75078. CrossRefGoogle Scholar
  52. Muschetto E, Mazia N, Cueto GR, Busch M (2015) Are rodents a source of biotic resistance to tree invasion in Pampean grasslands? Tree seed consumption under different conditions. Austral Ecol 40:255–266. CrossRefGoogle Scholar
  53. Nagelkerke NJ (1991) A note on a general definition of the coefficient of determination. Biometrika 78:691–692. CrossRefGoogle Scholar
  54. Niinemets Ü (2010) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25:693–714. CrossRefGoogle Scholar
  55. Nuñez MA, Simberloff D, Relva MA (2008) Seed predation as a barrier to alien conifer invasions. Biol Invasions 10:1389–1398CrossRefGoogle Scholar
  56. Oje K, Ugbor EC (1991) Some physical properties of oil bean seed. J Agric Eng Res 50:305–313. CrossRefGoogle Scholar
  57. Orrock JL et al (2015) A continent-wide study reveals clear relationships between regional abiotic conditions and post-dispersal seed predation. J Biogeogr 42:662–670. CrossRefGoogle Scholar
  58. Ortega YK, Pearson DE, Waller LP, Sturdevant NJ, Maron JL (2012) Population-level compensation impedes biological control of an invasive forb and indirect release of a native grass. Ecology 93:783–792CrossRefGoogle Scholar
  59. Ostoja SM, Schupp E, Klinger R (2013) Seed harvesting by a generalist consumer is context-dependent: Interactive effects across multiple spatial scales. Oikos 122:563–574. CrossRefGoogle Scholar
  60. Ostoja SM, Schupp EW, Durham S, Klinger R (2013) Seed harvesting is influenced by associational effects in mixed seed neighbourhoods, not just by seed density. Funct Ecol 27:775–785. CrossRefGoogle Scholar
  61. Pardiñas UFJ, Teta P (2013) Holocene stability and recent dramatic changes in micromammalian communities of northwestern Patagonia. Quatern Int 305:127–140. CrossRefGoogle Scholar
  62. Pearson OP (1983) Characteristics of a mammalian fauna from forests in Patagonia, Southern Argentina. J Mammal 64(3):476–492CrossRefGoogle Scholar
  63. Pearson OP (1995) Annotated keys for identifying small mammals living in or near Nahuel Huapi National Park or Lanin National Park, Southern Argentina. Mastozool Neotrop 2:99–148Google Scholar
  64. Pearson DE, Callaway RM, Maron JL (2011) Biotic resistance via granivory: establishment by invasive, naturalized, and native asters reflects generalist preference. Ecology 92:1748–1757CrossRefGoogle Scholar
  65. Pfister CA, Hay ME (1988) Associational plant refuges: convergent patterns in marine and terrestrial communities result from differing mechanisms. Oecologia 77:118–129. CrossRefGoogle Scholar
  66. Pirk GI, Lopez de Casenave J (2017) Ant interactions with native and exotic seeds in the Patagonian steppe: Influence of seed traits, disturbance levels and ant assemblage. Plant Ecol 218:1255–1268. CrossRefGoogle Scholar
  67. R Core Team (2018) R: A language and environment for statistical computing. Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  68. Raffaele E, Nuñez MA, Eneström J, Blackhall M (2016) Fire as mediator of pine invasion: evidence from Patagonia, Argentina. Biol Invasions 18:597–601. CrossRefGoogle Scholar
  69. Rejmánek M (1996) A theory of seed plant invasiveness: The first sketch. Biol Cons 78:171–181. CrossRefGoogle Scholar
  70. Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661. CrossRefGoogle Scholar
  71. Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species—2013 update of the global database. Divers Distrib 19:1093–1094. CrossRefGoogle Scholar
  72. Rejmánek, (2000) Invasive plants: approaches and predictions. Austral Ecol 25:497–506. CrossRefGoogle Scholar
  73. Rey PJ, Gutiérrez JE, Alcántara J, Valera F (1997) Fruit size in wild olives: implications for avian seed dispersal. Funct Ecol 11:611–618. CrossRefGoogle Scholar
  74. Richardson DM (2006) Pinus: a model group for unlocking the secrets of alien plant invasions? Preslia 78:375–388Google Scholar
  75. Richardson DM, Rejmánek M (2004) Conifers as invasive aliens: a global survey and predictive framework. Divers Distrib 10:321–331. CrossRefGoogle Scholar
  76. Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809. CrossRefGoogle Scholar
  77. Richardson DM, Cowling RM, Le Maitre DC (1990) Assessing the risk of invasive success in Pinus and Banksia in South African mountain fynbos. J Veg Sci 1:629–642. CrossRefGoogle Scholar
  78. Richardson DM, Williams PA, Hobbs RJ (1994) Pine invasions in the southern hemisphere: determinants of spread and invadability. J Biogeogr 21:511–527. CrossRefGoogle Scholar
  79. Rubino FM et al (2012) Food choice of Eurasian red squirrels and concentrations of anti-predatory secondary compounds. Mamm Biol 77:332–338. CrossRefGoogle Scholar
  80. Rueda M, Godoy O, Hawkins BA (2017) Spatial and evolutionary parallelism between shade and drought tolerance explains the distributions of conifers in the conterminous United States. Glob Ecol Biogeogr 26:31–42. CrossRefGoogle Scholar
  81. Sarasola M, Rusch V, Schlichter T, Ghersa C (2006) Tree conifers invasion in steppe areas and Austrocedus chilensis forests in NW Patagonia. Ecologia Austral 16:143–156Google Scholar
  82. Schlichter T, Laclau P (1998) Ecotono estepa-bosque y plantaciones forestales en la Patagonia norte. Ecologia Austral 8:285–296Google Scholar
  83. Simberloff D (2013) Invasive Species: What Everyone Needs to Know. Oxford University Press, New YorkGoogle Scholar
  84. Simberloff D, Relva MA, Nuñez M (2002) Gringos En El Bosque: introduced tree invasion in a native Nothofagus/Austrocedrus Forest. Biol Invasions 4:35–53. CrossRefGoogle Scholar
  85. Simberloff D et al (2010) Spread and impact of introduced conifers in South America: lessons from other southern hemisphere regions. Austral Ecol 35:489–504. CrossRefGoogle Scholar
  86. Swope SM, Parker IM (2010) Widespread seed limitation affects plant density but not population trajectory in the invasive plant Centaurea solstitialis. Oecologia 164:117–128. CrossRefGoogle Scholar
  87. Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346. CrossRefGoogle Scholar
  88. van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. CrossRefGoogle Scholar
  89. van Kleunen M, Dawson W, Maurel N (2015) Characteristics of successful alien plants. Mol Ecol 24:1954–1968. CrossRefGoogle Scholar
  90. Wang B, Ives AR (2017) Tree-to-tree variation in seed size and its consequences for seed dispersal versus predation by rodents. Oecologia 183:751–762. CrossRefGoogle Scholar
  91. Wang Z, Cao L, Zhang Z (2014) Seed traits and taxonomic relationships determine the occurrence of mutualisms versus seed predation in a tropical forest rodent and seed dispersal system. Integr Zool 9:309–319. CrossRefGoogle Scholar
  92. Wheelwright NT (1985) Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818. CrossRefGoogle Scholar
  93. Wheelwright NT (1993) Fruit size in a tropical tree species: variation, preference by birds, and heritability. Vegetatio 107:163–174. Google Scholar
  94. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666. CrossRefGoogle Scholar
  95. Wood DM, Andersen MC (1990) The effect of predispersal seed predators on colonization of Aster ledophyllus on Mount St. Helens Washington. Am Midl Nat 123:193–201. CrossRefGoogle Scholar
  96. Zhang H, Zhang Z (2008) Endocarp thickness affects seed removal speed by small rodents in a warm-temperate broad-leafed deciduous forest, China. Acta Oecologica 34:285–293. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Grupo de Ecología de Invasiones, INIBIOMAUniversidad Nacional del Comahue, CONICETSan Carlos de BarilocheArgentina

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