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Plant Ecology

, Volume 220, Issue 4–5, pp 541–552 | Cite as

A trade-off between primary and secondary seed dispersal by wind

  • Jinlei ZhuEmail author
  • Minghu Liu
  • Zhiming Xin
  • Zhimin Liu
  • Frank M. Schurr
Article

Abstract

The seeds of most plant species are dispersed by multiple mechanisms. Whether functional traits mediate positive correlations or negative correlations (trade-offs) between different dispersal mechanisms has important consequences for ecological and evolutionary dynamics. We investigate how traits affect wind-driven seed dispersal through the air and across the ground (primary and secondary wind dispersal, respectively). We hypothesized that primary and secondary wind dispersal were positively correlated because they should both decrease with the wing loading of seeds. We test this hypothesis with wind-tunnel experiments using different seed morphologies of Zygophyllum xanthoxylon (heterocarpous) and Calligonum species. We measured primary dispersal distance at varying wind speeds and release heights, and quantified secondary dispersal potential as the threshold wind speed for seed movement on four ground surfaces. Contrary to our expectation, we found a context-dependent trade-off between primary and secondary wind dispersal. The smoother the ground surface, the stronger this trade-off becomes. The trade-off results from a positive relationship between wing loading and the ratio of vertical to horizontal seed projection (v/h-ratio): an increasing v/h-ratio not only promotes secondary dispersal on smooth surfaces by increasing wind interception of seeds, but also decreases primary dispersal distance by increasing wing loading and terminal velocity of seeds. The trade-off contradicts the widespread assumption of a positive correlation between primary and secondary dispersal. A simple classification into poorly and well-dispersed seeds is thus not possible. The trade-off may affect dynamics of succession and the expansion of pioneer vegetation, while potentially slowing down evolutionary responses to selection on seed dispersal.

Keywords

Anemochory Diaspore Dispersal evolution Experimental ecology Functional traits Plant dispersal 

Notes

Acknowledgements

Thanks to Yaru Huang and Batu Gegen for assistance with seed collection, to Baoqing Liu, Xinle Li, Yingbin Ma and Yingming Zhao for assistance with dispersal experiments, and to two anonymous reviewers for helpful comments on the manuscript. The work was supported by the National Natural Science Foundation of China (NSFC) [41571270], the Sino-German (CSC-DAAD) Postdoc Scholarship Program [57165010], and the German Research Foundation (DFG) [DynNiche, SCHU 2259/5-1].

Supplementary material

11258_2019_934_MOESM1_ESM.docx (496 kb)
Supplementary file1 (DOCX 495 kb)

References

  1. Andersen MC (1993) Diaspore morphology and seed dispersal in several wind-dispersed Asteraceae. Am J Bot 80:487–492.  https://doi.org/10.1002/j.1537-2197.1993.tb13830.x CrossRefGoogle Scholar
  2. Augspurger CK (1986) Morphology and dispersal potential of wind-dispersed diaspores of neotropical trees. Am J Bot 73:353–363.  https://doi.org/10.2307/2444078 CrossRefGoogle Scholar
  3. Barton K (2018) MuMIn: multi-model inference. https://CRAN.R-project.org/package=MuMIn. Accessed 31 Jan 2018
  4. Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R package version 1:1–7.  https://doi.org/10.18637/jss.v067.i01 Google Scholar
  5. Brandel M (2007) Ecology of achene dimorphism in Leontodon saxatilis. Ann Bot 100:1189–1197.  https://doi.org/10.1093/aob/mcm214 CrossRefGoogle Scholar
  6. Chambers JC, MacMahon JA (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annu Rev Ecol Syst 25:263–292.  https://doi.org/10.1146/annurev.es.25.110194.001403 CrossRefGoogle Scholar
  7. Cheptou PO, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Natl Acad Sci USA 105:3796–3799.  https://doi.org/10.1073/pnas.0708446105 CrossRefGoogle Scholar
  8. Couvreur M, Verheyen K, Hermy M (2005) Experimental assessment of plant seed retention times in fur of cattle and horse. Flora-Morphology, Distribution, Functional Ecology of Plants 200:136–147.  https://doi.org/10.1016/j.flora.2004.06.003 CrossRefGoogle Scholar
  9. Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418:700–707.  https://doi.org/10.1038/nature01019 CrossRefGoogle Scholar
  10. Estrada A, Morales-Castilla I, Caplat P, Early R (2016) Usefulness of species traits in predicting range shifts. Trends Ecol Evol 31:190–203.  https://doi.org/10.1016/j.tree.2015.12.014 CrossRefGoogle Scholar
  11. Fuller DQ, Allaby R (2009) Seed dispersal and crop domestication: Shattering, germination and seasonality in evolution under cultivation. In: Østergaard L (ed) Annual Plant Reviews Volume 38: Fruit Development and Seed Dispersal. Wiley-Blackwell, pp 238–295.  https://doi.org/10.1002/9781444314557.ch7 CrossRefGoogle Scholar
  12. Greene DF, Johnson EA (1989) A model of wind dispersal of winged or plumed seeds. Ecology 70:339–347.  https://doi.org/10.2307/1937538 CrossRefGoogle Scholar
  13. Greene DF, Johnson EA (1990) The aerodynamics of plumed seeds. Funct Ecol 4:117–125.  https://doi.org/10.2307/2389661 CrossRefGoogle Scholar
  14. Greene DF, Johnson EA (1997) Secondary dispersal of tree seeds on snow. J Ecol 85:329–340.  https://doi.org/10.2307/2960505 CrossRefGoogle Scholar
  15. Jakobsson A, Eriksson O (2003) Trade-offs between dispersal and competitive ability: a comparative study of wind-dispersed Asteraceae forbs. Evol Ecol 17:233–246.  https://doi.org/10.1023/A:1025526903281 CrossRefGoogle Scholar
  16. Johnson EA, Fryer GI (1992) Physical characterization of seed microsites - movement on the ground. J Ecol 80:823–836.  https://doi.org/10.2307/2260869 CrossRefGoogle Scholar
  17. Jongejans E, Telenius A (2001) Field experiments on seed dispersal by wind in ten umbelliferous species (Apiaceae). Plant Ecol 152:67–78.  https://doi.org/10.1023/a:1011467604469 CrossRefGoogle Scholar
  18. Jumpponen A, Väre H, Mattson KG, Ohtonen R, Trappe JM (1999) Characterization of ‘safe sites’ for pioneers in primary succession on recently deglaciated terrain. J Ecol.  https://doi.org/10.1046/j.1365-2745.1999.00328.x Google Scholar
  19. Kowarik I, von der Lippe M (2011) Secondary wind dispersal enhances long-distance dispersal of an invasive species in urban road corridors. NeoBiota 9:49–70.  https://doi.org/10.3897/neobiota.9.1469 CrossRefGoogle Scholar
  20. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226.  https://doi.org/10.1111/j.1558-5646.1983.tb00236.x CrossRefGoogle Scholar
  21. Levin SA, Muller-Landau HC, Nathan R, Chave J (2003) The ecology and evolution of seed dispersal: A theoretical perspective. Annu Rev Ecol Evol Syst 34:575–604.  https://doi.org/10.1146/annurev.ecolsys.34.011802.132428 CrossRefGoogle Scholar
  22. Martínez-Garza C, Flores-Palacios A, De La Pena-Domene M, Howe HF (2009) Seed rain in a tropical agricultural landscape. J Trop Ecol 25:541–550.  https://doi.org/10.1017/S0266467409990113 CrossRefGoogle Scholar
  23. Monteith JL, Unsworth MH (2013) Micrometeorology: (i) turbulent transfer, profiles, and fluxes. In: Monteith JL, Unsworth MH (eds) Principles of environmental physics, 4th edn. Academic Press, Boston, pp 289-320.  https://doi.org/10.1016/B978-0-12-386910-4.00016-0 CrossRefGoogle Scholar
  24. Nathan R, Safriel UN, Noy-Meir I (2001) Field validation and sensitivity analysis of a mechanistic model for tree seed dispersal by wind. Ecology 82:374–388.  https://doi.org/10.1890/0012-9658(2001)082[0374:fvasao]2.0.co;2 CrossRefGoogle Scholar
  25. Nathan R et al (2002) Mechanisms of long-distance dispersal of seeds by wind. Nature 418:409–413.  https://doi.org/10.1038/nature00844 CrossRefGoogle Scholar
  26. Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. Trends Ecol Evol 23:638–647.  https://doi.org/10.1016/j.tree.2008.08.003 CrossRefGoogle Scholar
  27. Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285.  https://doi.org/10.1016/s0169-5347(00)01874-7 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 RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI. pp 252-276.  https://doi.org/10.1079/9781845931650.0252 CrossRefGoogle Scholar
  29. Norberg R (1973) Autorotation, self-stability, and structure of single-winged fruits and seeds (samaras) with comparative remarks on animal flight. Biol Rev 48:561–596.  https://doi.org/10.1111/j.1469-185X.1973.tb01569.x CrossRefGoogle Scholar
  30. Pounden E, Greene D, Quesada M, Contreras Sánchez JM (2008) The effect of collisions with vegetation elements on the dispersal of winged and plumed seeds. J Ecol 96:591–598.  https://doi.org/10.1111/j.1365-2745.2008.01380.x CrossRefGoogle Scholar
  31. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  32. Redbo-Torstensson P, Telenius A (1995) Primary and secondary seed dispersal by wind and water in Spergularia salina. Ecography 18:230–237.  https://doi.org/10.1111/j.1600-0587.1995.tb00126.x CrossRefGoogle Scholar
  33. Ronce O, Brachet S, Olivieri I, Gouyon PH, Clobert J (2005) Plastic changes in seed dispersal along ecological succession: theoretical predictions from an evolutionary model. J Ecol 93:431–440.  https://doi.org/10.1111/j.1365-2745.2005.00972.x CrossRefGoogle Scholar
  34. Rubio de Casas R, Willis CG, Donohue K (2012) Plant dispersal phenotypes: a seed perspective of maternal habitat selection. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp 171–184CrossRefGoogle Scholar
  35. 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.  https://doi.org/10.1111/j.1365-2745.2005.01018.x CrossRefGoogle Scholar
  36. Schurr FM, Steinitz O, Nathan R (2008) Plant fecundity and seed dispersal in spatially heterogeneous environments: models, mechanisms and estimation. J Ecol 96:628–641.  https://doi.org/10.1111/j.1365-2745.2008.01371.x CrossRefGoogle Scholar
  37. Sheldon JC, Burrows FM (1973) The dispersal effectiveness of the achene-pappus units of selected Compositae in steady winds with convection. New Phytol 72:665–675.  https://doi.org/10.1111/j.1469-8137.1973.tb04415.x CrossRefGoogle Scholar
  38. Soons MB, Heil GW, Nathan R, Katul GG (2004) Determinants of long-distance seed dispersal by wind in grasslands. Ecology 85:3056–3068.  https://doi.org/10.1890/03-0522 CrossRefGoogle Scholar
  39. Sutherland WJ et al (2013) Identification of 100 fundamental ecological questions. J Ecol 101:58–67.  https://doi.org/10.1111/1365-2745.12025 CrossRefGoogle Scholar
  40. Svenning JC et al (2014) The influence of interspecific interactions on species range expansion rates. Ecography 37:1198–1209.  https://doi.org/10.1111/j.1600-0587.2013.00574.x CrossRefGoogle Scholar
  41. Tackenberg O, Römermann C, Thompson K, Poschlod P (2006) What does diaspore morphology tell us about external animal dispersal? Evidence from standardized experiments measuring seed retention on animal-coats. Basic Appl Ecol 7:45–58.  https://doi.org/10.1016/j.baae.2005.05.001 CrossRefGoogle Scholar
  42. Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16.  https://doi.org/10.2307/1939377 CrossRefGoogle Scholar
  43. van Tooren BF (1988) The fate of seeds after dispersal in chalk grassland: the role of the bryophyte layer. Oikos 53:41–48.  https://doi.org/10.2307/3565661 CrossRefGoogle Scholar
  44. Vander Wall SB (2003) Effects of seed size of wind-dispersed pines (Pinus) on secondary seed dispersal and the caching behavior of rodents. Oikos 100:25–34.  https://doi.org/10.1034/j.1600-0706.2003.11973.x CrossRefGoogle Scholar
  45. von der Lippe M, Bullock JM, Kowarik I, Knopp T, Wichmann MC (2013) Human-mediated dispersal of seeds by the airflow of vehicles. PLoS ONE 8:e52733.  https://doi.org/10.1371/journal.pone.0052733 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute of Landscape and Plant EcologyUniversity of HohenheimStuttgartGermany
  2. 2.Experimental Center of Desert ForestryChinese Academy of ForestryDengkouChina
  3. 3.Institute of Applied EcologyChinese Academy of SciencesShenyangChina

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