Abstract
Negative correlations between dispersal and establishment are often reported in the plant literature; smaller seeds tend to disperse better but germinate less well, and produce smaller seedlings. However, because dispersal capacity is often quantified using proxies, such as the settling velocity of wind-dispersed seeds, little is known about the exact shape of this negative relationship, and how it is modified by other plant traits and environmental conditions. We studied the dispersal-establishment relationship in two wind-dispersed thistles (Carduus nutans and Carduus acanthoides). We applied a mechanistic wind dispersal model (WALD) to seeds released under a range of environmental conditions, and tested germination and seedling growth under standardized conditions in a greenhouse. Dispersal distance and establishment (germination and seedling growth) were not significantly correlated, although in both species smaller seeds dispersed farther, and showed lower germination and lower seedling growth rates. This apparent paradox can partly be explained by the significant influence of other factors such as release height and environment (wind and vegetation), which explained more variation in dispersal than did terminal velocity. Another potential explanation is the variation in seed traits: germination is strongly positively related to seed mass, weakly positively related to plume loading, but not significantly related to terminal velocity. This weakening of the correlation with germination is due to additional layers of trait (co)variability: for instance, seed mass and pappus size are positively correlated, and thus big seeds partially compensate for the negative effect of seed mass with larger pappi. Our mechanistic approach can thus lead to a better understanding of both potentially opposing selection pressures on traits like seed mass, and diluting effects of other seed, plant and environmental factors.
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References
Allen MR, Shea K (2006) Spatial segregation of congeneric invaders in central Pennsylvania, USA. Biol Invas 8:509–521
Andersen M (1993) Diaspore morphology and seed dispersal in several wind-dispersed Asteraceae. Am J Bot 80:487–492
Bullock JM (2000) Gaps and seedling colonization. In: Fenner MJ (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CAB International, Wallingford, pp 375–395
Bullock JM, Hill BC, Silvertown J, Sutton M (1995) Gap colonization as a source of grassland community change: effects of gap size and grazing on the rate and mode of colonization by different species. Oikos 72:273–282
Coomes DA, Grubb PJ (2003) Colonization, tolerance, competition and seed-size variation within functional groups. Trends Ecol Evol 18:283–291
Debain S, Curt T, Lepart J (2003) Seed mass, seed dispersal capacity, and seedling performance in a Pinus sylvestris population. Ecoscience 10:168–175
Desrochers AM, Bain JF, Warwick SI (1988) The biology of Canadian weeds. 89. Carduus nutans L. and Carduus acanthoides L. Can J Plant Sci 68:1053–1068
Evans M, Hastings N, Peacock B (2000) Statistical distributions. Wiley, New York
Geritz SAH, de Jong TJ, Klinkhamer PGL (1984) The efficacy of dispersal in relation to safe site area and seed production. Oecologia 62:219–221
Greene DF, Johnson EA (1990) The aerodynamics of plumed seeds. Funct Ecol 4:117–125
Greene DF, Johnson EA (1993) Seed mass and dispersal capacity in wind-dispersed diaspores. Oikos 67:69–74
Greene DF, Quesada M (2005) Seed size, dispersal, and aerodynamic constraints within the Bombacaceae. Am J Bot 92:998–1005
Holm L, Pancho JV, Herberger JP, Plucknett DL (1979) A geographical atlas of world weeds. Wiley, New York
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
Jongejans E, Pedatella N, Shea K, Skarpaas O, Auhl R (2007a) Seed release by invasive thistles: the impact of plant and environmental factors. Proc Royal Soc B Biol Sci 274:2457–2464
Jongejans E, Skarpaas O, Tipping PW, Shea K (2007b) Establishment and spread of founding populations of an invasive thistle: the role of competition and seed limitation. Biol Invasions 9:317–325
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
Katul GG et al (2005) Mechanistic analytical models for long-distance seed dispersal by wind. Am Nat 166:368–381
Knops JMH, Koenig WD, Carmen WJ (2007) Negative correlation does not imply a tradeoff between growth and reproduction in California oaks. Proc Nat Acad Sci 104:16982–16985
Kuparinen A (2006) Mechanistic models for wind dispersal. Trends Plant Sci 11:297–301
Marchetto KM, Jongejans E, Jennis ML, Haner EM, Sullivan CT, Shea K (2010a) Shipment and storage effects on the terminal velocity of seeds. Ecol Res 25:83–92
Marchetto KM, Jongejans E, Shea K, Isard SA (2010b) Patch characteristics affect projected invasion speed. Oikos. doi:10.1111/j.1600-0706.2010.18329.x
Matlack GR (1987) Diaspore size, shape and fall behavior in wind-dispersed plant species. Am J Bot 74:1150–1160
Mazer SJ, Wolfe LM (1992) Planting density influences the expression of genetic variation in seed mass in wild radish (Raphanus sativus L.: Brassicaceae). Am J Bot 79:1185–1193
McCarty MK, Scifres CJ, Smith AL, Horst GL (1969) Germination and early seedling development of musk and plumeless thistles. In: Research Bulletin. College of Agriculture and Home Economics, University of Nebraska, pp 1–28
Metcalf CJE, Rees M, Buckley YM, Sheppard AW (2009) Seed predators and the evolutionary stable flowering strategy in the invasive plant, Carduus nutans. Evol Ecol 23:893–906
Meyer SE, Carlson SL (2001) Achene mass variation in Ericameria nauseosus (Asteraceae) in relation to dispersal ability and seedling fitness. Funct Ecol 15:274–281
Nathan R et al (2002) Mechanisms of long-distance dispersal of seeds by wind. Nature 418:409–413
R Development Core Team (2009) R: A language and environment for statistical computing, 2.9.0 edn. R Foundation for Statistical Computing, Vienna, Austria
Sakai S, Kikuzawa K, Umeki K (1998) Evolutionarily stable resource allocation for production of wind-dispersed seeds. Evol Ecol 12:477–485
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
Shea K, Kelly D (1998) Estimating biocontrol agent impact with matrix models: Carduus nutans in New Zealand. Ecol Appl 8:824–832
Shea K, Kelly D, Sheppard AW, Woodburn TL (2005) Context-dependent biological control of an invasive thistle. Ecology 86:3174–3181
Shea K, Sheppard A, Woodburn T (2006) Seasonal life history models for the integrated management of the invasive weed nodding thistle (Carduus nutans) in Australia. J Appl Ecol 43:517–526
Skarpaas O, Shea K (2007) Dispersal patterns, dispersal mechanisms and invasion wave speeds for invasive thistles. Am Nat 170:421–430
Skarpaas O, Auhl R, Shea K (2006) Environmental variability and the initiation of dispersal: turbulence strongly increases seed release. Proc Royal Soc Lond Series B 273:751–756
Soons MB, Heil G (2002) Reduced colonization capacity in fragmented populations of wind-dispersed grassland forbs. J Ecol 90:1033–1043
Stratton DA (1989) Competition prolongs expression of maternal effects in seedlings of Erigeron annuus (Asteraceae). Am J Bot 76:1646–1653
Strykstra RJ, Pegtel DM, Bergsma A (1998) Dispersal distance and achene quality of the rare anemochorous species Arnica montana L.: implications for conservation. Acta Bot Neerland 47:45–56
Turnbull LA, Rees M, Crawley MJ (1999) Seed mass and the competition/colonization trade-off: a sowing experiment. J Ecol 87:899–912
Turnbull LA, Coomes D, Hector A, Rees M (2004) Seed mass and the competition/colonization trade-off: competitive interactions and spatial patterns in a guild of annual plants. J Ecol 92:97–109
Wheelwright NT (1993) Fruit size in a tropical tree species: variation, preference by birds, and heritability. Plant Ecol 107–108:163–174
Acknowledgments
We are grateful to Jeff Buterbaugh, Paul Chen, Matt Clark, Wilmer Garman, Brian Jones, Pete LeVan, Melanie Northrup, Emily Leichtman, Emily Rauschert, Christina Saylor, Zeynep Sezen and Laura Warg for assistance in field and lab studies, and to two anonymous reviewers for valuable comments. This work was funded by the National Science Foundation (grant no. DEB-0315860 and DEB-0614065 to KS), the Norwegian Research Council (grant no. 161484/V10 to OS) and the Netherlands Organization for Scientific Research (NWO veni-grant 863.08.006 to EJ).
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Skarpaas, O., Silverman, E.J., Jongejans, E. et al. Are the best dispersers the best colonizers? Seed mass, dispersal and establishment in Carduus thistles. Evol Ecol 25, 155–169 (2011). https://doi.org/10.1007/s10682-010-9391-4
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DOI: https://doi.org/10.1007/s10682-010-9391-4