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Ecological Research

, Volume 30, Issue 1, pp 173–180 | Cite as

Post-dispersal seed removal of Carduus nutans and C. acanthoides by insects and small mammals

  • Eelke JongejansEmail author
  • Edward J. Silverman
  • Olav Skarpaas
  • Katriona Shea
Original Article

Abstract

The journey of wind-dispersed seeds does not necessarily end when they land. Secondary dispersal and/or predation can positively or negatively affect the spread of invasive plants. Here we studied post-dispersal seed removal of nodding and plumeless thistle (Carduus nutans and C. acanthoides) in part of their invaded range in Pennsylvania, USA. The relative impact of small mammals and insects was determined using exclusion treatments in the field. In cages that allowed insect access, 88 % of the seeds were removed after 1 day, and 99.9 % were removed after the 6-day trial. When insects were excluded, the removal rate was significantly lower (18 % after 1 day, 40 % after 6 days). The seed removal rates provide an upper limit to the seed predation rate, with the understanding that it is also possible for seed removal to be an important secondary dispersal mechanism. We discuss a combined empirical-theoretical approach to evaluate the impact of these alternative seed fates on the spread and management of these thistles.

Keywords

Animal seed removers Invasive thistle species Predation Secondary (serial) dispersal Seed size Seed removal 

Notes

Acknowledgments

Emily Rauschert and Zeynep Sezen provided thoughtful contributions to the experimental design and procedures. Candace Davison lent her expertise in gamma irradiation and conducted the seed irradiations. Sarah Perkins was helpful in identifying small mammals at the field site. Jessie Blake Lough, Steven Selego and Evin Brown assisted in the field. Sarah Assman and 3 anonymous reviewers provided useful comments on the manuscript. This research was partly funded by the National Science Foundation (Grant DEB-0315860). E.J.S. received funding from the PSU Schreyer Honors College.

Supplementary material

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References

  1. Abbott I, van Heurck P (1985) Comparison of insects and vertebrates as removers of seed and fruit in a Western Australian forest. Aust J Ecol 10:165–168. doi: 10.1111/j.1442-9993.1985.tb00877.x CrossRefGoogle Scholar
  2. 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 210:291–301. doi: 10.1007/s11258-010-9757-2 CrossRefGoogle Scholar
  3. Allen MR, Shea K (2006) Spatial segregation of congeneric invaders in central Pennsylvania, USA. Biol Invasions 8:509–521. doi: 10.1007/s10530-005-6407-z CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B (2013) lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-2. http://CRAN.R-project.org/package=lme4
  5. Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639. doi: 10.1038/35098093 PubMedCrossRefGoogle Scholar
  6. Desrochers AM, Bain JF, Warwick SI (1988) A biosystematic study of the Carduus nutans complex in Canada. Can J Bot 66:1621–1631. doi: 10.1139/b88-221 CrossRefGoogle Scholar
  7. Gallegos SC, Hensen I, Schleuning M (2014) Secondary dispersal by ants promotes forest regeneration after deforestation. J Ecol 102:659–666. doi: 10.1111/1365-2745.12226 CrossRefGoogle Scholar
  8. Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 3:481–492. doi: 10.1111/j.0030-1299.2006.14258.x CrossRefGoogle Scholar
  9. Gómez C, Espadaler X (1998) Seed dispersal curve of a Mediterranean myrmecochore: influence of ant size and the distance to nests. Ecol Res 13:347–354CrossRefGoogle Scholar
  10. Hammond DS (1995) Post-dispersal seed and seedling mortality of tropical dry forest trees after shifting agriculture, Chiapas, Mexico. J Trop Ecol 11:295–313CrossRefGoogle Scholar
  11. Harrison SK, Regnier EE, Schmoll JT (2003) Postdispersal predation of giant ragweed (Ambrosia trifida) seed in no-tillage corn. Weed Sci 51:955–964CrossRefGoogle Scholar
  12. Heggenstaller AH, Menalled FD, Liebman M, Westerman PR (2006) Seasonal patterns in post-dispersal seed predation of Abutilon theophrasti and Setaria faberi in three cropping systems. J Appl Ecol 43:999–1010CrossRefGoogle Scholar
  13. Howe HF (1986) Seed dispersal by fruit eating birds and mammals. In: Murray DR (ed) Seed dispersal. Academic Press, New York, pp 123–189Google Scholar
  14. Hughes L, Westoby M (1992) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299CrossRefGoogle Scholar
  15. Hulme PE (1997) Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111:91–98CrossRefGoogle Scholar
  16. Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol Evol Syst 1:32–46CrossRefGoogle Scholar
  17. Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecol Monogr 74:569–589CrossRefGoogle Scholar
  18. Jansen PA, Hirsch BT, Emsens W-J, Zamora-Gutierrez V, Wikelski M, Kays R (2012) Thieving rodents as substitute dispersers of megafaunal seeds. Proc Nat Acad Sci USA 109:12610–12615. doi: 10.5441/001/1.9t0m888q PubMedCentralPubMedCrossRefGoogle Scholar
  19. Jongejans E, Shea K, Skarpaas O, Kelly D, Sheppard AW, Woodburn TL (2008) Dispersal and demography contributions to population spread of Carduus nutans in its native and invaded ranges. J Ecol 96:687–697. doi: 10.1111/j.1365-2745.2008.01367.x CrossRefGoogle Scholar
  20. Jongejans E, Allen MR, Leib AE, Marchetto KM, Pedatella NM, Peterson-Smith J, Rauschert ESJ, Ruggiero DC, Russo LA, Ruth LE, Sezen Z, Skarpaas O, Teller BJ, Warg LA, Yang S, Zhang R, Shea K (2011) Spatial dynamics of invasive Carduus thistles. In: Chan F, Marinova D, Anderssen RS (eds) MODSIM2011, 19th international congress on modelling and simulation. Modelling and simulation society of Australia and New Zealand, pp 2514–2520Google Scholar
  21. Kelly D, McCallum K (1990) Demography, seed biology and biological control of Carduus nutans in New Zealand. In: Palmer JP (ed) The biology and control of invasive plants. British Ecological Society, Cardiff, pp 72–79Google Scholar
  22. Kollmann J, Bassin S (2001) Effects of management on seed predation in wildflower strips in northern Switzerland. Agric Ecosyst Environ 83:285–296CrossRefGoogle Scholar
  23. Kollmann J, Coomes DA, White SM (1998) Consistencies in post-dispersal seed predation of temperate fleshy-fruited species among seasons, years and sites. Funct Ecol 12:683–690CrossRefGoogle Scholar
  24. Marchetto KM, Jongejans E, Jennis ML, Haner EM, Sullivan CT, Kelly D, Shea K (2010) Shipment and storage effects on the terminal velocity of seeds. Ecol Res 25:83–92. doi: 10.1007/s11284-009-0634-1 CrossRefGoogle Scholar
  25. Marchetto KM, Shea K, Kelly D, Groenteman R, Sezen Z, Jongejans E (2014) Unrecognized impact of a biocontrol agent on the spread rate of an invasive thistle. Ecol Appl 24:1178–1187. doi: 10.1890/13-1309.1 PubMedCrossRefGoogle Scholar
  26. Mauchline AL, Watson SJ, Brown VK, Froud-Williams RJ (2005) Post-dispersal seed predation of non-target weeds in arable crops. Weed Res 45:157–164. doi: 10.1111/j.1365-3180.2004.00443.x CrossRefGoogle Scholar
  27. Moupela C, Doucet J-L, Daïnou K, Tagg N, Bourland N, Vermeulen C (2014) Dispersal and predation of diaspores of Coula edulis Baill. in an evergreen forest of Gabon. Afr J Ecol 52:88–96. doi: 10.1111/aje.12089 CrossRefGoogle Scholar
  28. Nathan R (2007) Total dispersal kernels and the evaluation of diversity and similarity in complex dispersal systems. In: Dennis AJ, Schupp EW, Green RA, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI, pp 252–276Google Scholar
  29. Neubert MG, Caswell H (2000) Demography and dispersal: calculation and sensitivity analysis of invasion speed for structured populations. Ecology 81:1613–1628. doi:101890/0012-9658(2000)081[1613:DADCAS]20CO;2CrossRefGoogle Scholar
  30. Ohnishi YK, Katayama N, Suzuki N (2013) Differential dispersal of Chamaesyce maculata seeds by two ant species in Japan. Plant Ecol 214:907–915. doi: 10.1007/s11258-013-0217-7 CrossRefGoogle Scholar
  31. O’Rourke ME, Heggenstaller AH, Liebman M, Rice ME (2006) Post-dispersal weed seed predation by invertebrates in conventional and low-external-input crop rotation systems. Agric Ecosyst Environ 116:280–288CrossRefGoogle Scholar
  32. Pemberton RW, Irving DW (1990) Elaiosomes on weed seeds and the potential for myrmecochory in naturalized plants. Weed Sci 38:615–619Google Scholar
  33. Peterson-Smith J, Shea K (2010) Seedling emergence and early survival of Carduus spp. in three habitats with press and pulse disturbances. J Torrey Bot Soc 137:287–296. doi: 10.3159/09-RA-070R1.1 CrossRefGoogle Scholar
  34. Pierce SM, Cowling RM (1991) Dynamics of soil-stored seed banks of six shrubs in fire-prone dune fynbos. J Ecol 79:731–747. doi: 10.2307/2260664 CrossRefGoogle Scholar
  35. Prior KM, Saxena K, Frederickson ME (2014) Seed handling behaviours of native and invasive seed-dispersing ants differentially influence seedling emergence in an introduced plant. Ecol Entomol 39:66–74. doi: 10.1111/een.12068 CrossRefGoogle Scholar
  36. Pufal G, Klein A-M (2013) Post-dispersal seed predation of three grassland species in a plant diversity experiment. J Plant Ecol 6:468–479. doi: 10.1093/jpe/rtt011 CrossRefGoogle Scholar
  37. 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
  38. Redbo-Torstensson P, Telenius A (1995) Primary and secondary seed dispersal by wind and water in Spergularia salina. Ecography 18:230–237. doi: 10.1111/j.1600-0587.1995.tb00126.x CrossRefGoogle Scholar
  39. Retana J, Picó FX, Rodrigo A (2004) Dual role of harvesting ants as seed predators and dispersers of a non-myrmechorous Mediterranean perennial herb. Oikos 105:377–385. doi: 10.1111/j.0030-1299.2004.12854.x CrossRefGoogle Scholar
  40. Rey PJ, Garrido JL, Alcántara JM, Ramirez JM, Aguilera A, García L, Manzaneda AJ, Fernández R (2002) Spatial variation in ant and rodent post-dispersal predation of vertebrate-dispersed seeds. Funct Ecol 16:773–781. doi: 10.1046/j.1365-2435.2002.00680.x CrossRefGoogle Scholar
  41. Schurr FM, Bond WJ, Midgley GF, Higgins SI (2005) A mechanistic model for secondary seed dispersal by wind and its experimental validation. J Ecol 93:1017–1028. doi: 10.1111/j.1365-2745.2005.01018.x CrossRefGoogle Scholar
  42. Sheppard AW, Cullen JM, Aeschlimann JP (1994) Predispersal seed predation on Carduus nutans (Asteraceae) in Southern Europe. Acta Oecol 15:529–541Google Scholar
  43. Skarpaas O, Shea K (2007) Dispersal patterns, dispersal mechanisms and invasion wave speeds for invasive thistles. Am Nat 170:421–430. doi: 10.1086/519854 PubMedCrossRefGoogle Scholar
  44. Skarpaas O, Silverman EJ, Jongejans E, Shea K (2010) Are the best dispersers the best colonizers? Seed mass, dispersal and establishment in Carduus thistles. Evol Ecol 25:155–169. doi: 10.1007/s10682-010-9391-4 CrossRefGoogle Scholar
  45. Terborgh J, Losos E, Riley MP, Riley MB (1993) Predation by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest. Vegetatio 107(108):375–386. doi: 10.1007/978-94-011-1749-4_26 Google Scholar
  46. Türke M, Heinze E, Andreas K, Svendsen SM, Gossner MM, Weisser WW (2010) Seed consumption and dispersal of ant-dispersed plants by slugs. Oecologia 163:681–693. doi: 10.1007/s00442-010-1612-6 PubMedCrossRefGoogle Scholar
  47. Vander Wall SB, Forget P-M, Lambert JE, Hulme PE (2005a) Seed fate pathways: filling the gap between parent and offspring. In: Forget P-M, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford, pp 1–8Google Scholar
  48. Vander Wall SB, Kuhn KM, Beck MJ (2005b) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806CrossRefGoogle Scholar
  49. Weiss FE (1908) The dispersal of fruits and seeds by ants. New Phytol 7:23–28CrossRefGoogle Scholar
  50. Wenny DG (2001) Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol Ecol Res 3:51–74Google Scholar
  51. Westerman PR, Wes JS, Kropff MJ, van der Werf W (2003) Annual losses of weed seeds due to predation in organic cereal fields. J Appl Ecol 40:824–836CrossRefGoogle Scholar
  52. Whelan CJ, Willson MF, Tuma CA, Souza-Pinto I (1991) Spatial and temporal patterns of postdispersal seed predation. Can J Bot 69:428–436CrossRefGoogle Scholar
  53. Yang S, Jongejans E, Yang S, Bishop JG (2011) The effect of consumers and mutualists of Vaccinium membranaceum at Mount St. Helens: dependence on successional context. PLoS One 6:e26094PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2014

Authors and Affiliations

  • Eelke Jongejans
    • 1
    Email author
  • Edward J. Silverman
    • 2
  • Olav Skarpaas
    • 3
  • Katriona Shea
    • 2
  1. 1.Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland ResearchRadboud University NijmegenNijmegenThe Netherlands
  2. 2.Department of Biology and IGDP in EcologyThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Norwegian Institute for Nature ResearchOsloNorway

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