Allometry in the terminal velocity – dispersal architecture relationship explains variation in dispersal and offspring provisioning strategies in wind dispersed Asteraceae species
Samiya Tabassum A B and Stephen P. Bonser A C
+ Author Affiliations
- Author Affiliations
A Ecology and Evolution Research Centre, School of Biological, Earth, and Environmental Sciences, UNSW Australia, Sydney, NSW 2052, Australia.
B Present address: School of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.
C Corresponding author. Email: s.bonser@unsw.edu.au
Australian Journal of Botany 65(2) 149-156 https://doi.org/10.1071/BT16180
Submitted: 4 September 2016 Accepted: 14 February 2017 Published: 14 March 2017
Abstract
Competition can simultaneously favour high dispersal ability (to transport offspring to more favourable habitats) and large seed size (to maximise offspring provisioning). In wind dispersed Asteraceae species, seeds are enclosed within an achene with hair-like projections from the achene form a pappus that acts as a parachute to aid in dispersal. There is potentially an allometric relationship between terminal velocity and pappus to achene volume ratio (dispersal architecture), with changes in dispersal architecture resulting in disproportionately high or low impacts on terminal velocity. We tested the hypothesis that competition induces shifts in dispersal architecture depending on the allometric relationship between terminal velocity and dispersal architecture. We estimated dispersal architecture of diaspores from seven wind dispersed Asteraceae species from environments with low and high neighbour densities. We also estimated diaspore terminal velocity for a subset of these species by recording drop time in a 2 m tube. Diaspores of one species had dispersal architecture promoting higher dispersal under high neighbour density, diaspores of two species had dispersal architecture promoting lower dispersal under high neighbour density, and dispersal architecture was not significantly different between high and low density environments for four of the species. Species showed a common allometric relationship between terminal velocity and dispersal architecture. The allometric relationship predicts dispersal architecture changes across environments differing in neighbour density. Species with dispersal architecture promoting higher dispersal under high neighbour density do so where small increases in dispersal architecture yield large decreases in terminal velocity. Our research suggests that the nature of allometric relationships between traits can help to explain allocation strategies across environments.
Additional keywords: achene size, competition, pappus size, trade-offs, wind dispersal.
References
Alsos IG, Eidesen PB, Ehrich D, Skrede I, Westergaard K, Jacobsen GH, Landvik JY, Taberlet P, Brochmann C (2007) Frequent long-distance plant colonization in the changing Arctic. Science 316, 1606–1609.| Frequent long-distance plant colonization in the changing Arctic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtl2jsL4%3D&md5=78b477e58136eb66aa4fe7710246ac21CAS |
Andersen M (1992) An analysis of variability in seed settling velocities of several wind-dispersed Asteraceae. American Journal of Botany 79, 1087–1091.
| An analysis of variability in seed settling velocities of several wind-dispersed Asteraceae.Crossref | GoogleScholarGoogle Scholar |
Andersen M (1993) Diaspore morphology and seed dispersal in several wind-dispersed Asteraceae. American Journal of Botany 80, 487–492.
| Diaspore morphology and seed dispersal in several wind-dispersed Asteraceae.Crossref | GoogleScholarGoogle Scholar |
Bartle K, Moles AT, Bonser SP (2013) Rapid evolution of seed dispersal at the invasion fronts of the invasive species Senecio madagascariensis. Austral Ecology 38, 915–920.
| Rapid evolution of seed dispersal at the invasion fronts of the invasive species Senecio madagascariensis.Crossref | GoogleScholarGoogle Scholar |
Barton KA, Hovestadt T, Phillips BL, Travis JMJ (2012) Risky movement increases the rate of range expansion. Proceedings. Biological Sciences 279, 1194–1202.
| Risky movement increases the rate of range expansion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383hvVCitA%3D%3D&md5=d93bff5fe7e0686518ba92cdef219a9bCAS |
Baythavong BS, Stanton ML, Rice KJ (2009) Understanding the consequences of seed dispersal in a heterogeneous environment. Ecology 90, 2118–2128.
| Understanding the consequences of seed dispersal in a heterogeneous environment.Crossref | GoogleScholarGoogle Scholar |
Bergelson J, Newman JA, Floresroux EM (1993) Rates of weed spread in spatially heterogeneous environments. Ecology 74, 999–1011.
| Rates of weed spread in spatially heterogeneous environments.Crossref | GoogleScholarGoogle Scholar |
Charnov EL (1997) Trade-off-invariant rules for evolutionary stable life histories. Nature 387, 393–394.
| Trade-off-invariant rules for evolutionary stable life histories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsVeiur0%3D&md5=9a5a8baddd8ee42a25d45ac7c227bfb5CAS |
Cheptou PO, Carrue O, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proceedings of the National Academy of Sciences of the United States of America 105, 3796–3799.
| Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjslSiur4%3D&md5=9f18e8e38fc768ad4e013a607b7a95ecCAS |
Cody ML, Overton JM (1996) Short-term evolution of reduced dispersal in island plant populations. Journal of Ecology 84, 53–61.
| Short-term evolution of reduced dispersal in island plant populations.Crossref | GoogleScholarGoogle Scholar |
Coomes DA, Grubb PJ (2003) Colonization, tolerance, competition and seed size variation within functional groups. Trends in Ecology & Evolution 18, 283–291.
| Colonization, tolerance, competition and seed size variation within functional groups.Crossref | GoogleScholarGoogle Scholar |
Dytham C (2009) Evolved dispersal strategies at range margins. Proceedings. Biological Sciences 276, 1407–1413.
| Evolved dispersal strategies at range margins.Crossref | GoogleScholarGoogle Scholar |
Elisens WJ, Boyd RD, Wolfe AD (1992) Genetic and morphological divergence among varieties of Aphanostephus skirrhobasis (Asteraceae – Astereae) and related species with different chromosome numbers. Systematic Botany 17, 380–394.
| Genetic and morphological divergence among varieties of Aphanostephus skirrhobasis (Asteraceae – Astereae) and related species with different chromosome numbers.Crossref | GoogleScholarGoogle Scholar |
Enquist BJ, West GB, Charnov EL, Brown JH (1999) Allometric scaling of production and life-history variation in vascular plants. Nature 401, 907–911.
| Allometric scaling of production and life-history variation in vascular plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFyltr8%3D&md5=583360619985e339b47e7f878eb0365aCAS |
Falster DS, Warton D, Wright I (2006) ‘User’s guide to SMATR: standardised major axis tests and routines, ver. 2.0.’ Available at http://www.bio.mq.edu.au/ecology/SMATR [Verified 23 February 2017].
Ford H (1981) The demography of three populations of dandelion. Biological Journal of the Linnaean Society 15, 1–11.
| The demography of three populations of dandelion.Crossref | GoogleScholarGoogle Scholar |
Gravuer K, von Wettberg EJ, Schmitt J (2003) Dispersal biology of Liatris scariosa var. novae-angliae (Asteraceae), a rare New England grassland perennial. American Journal of Botany 90, 1159–1167.
| Dispersal biology of Liatris scariosa var. novae-angliae (Asteraceae), a rare New England grassland perennial.Crossref | GoogleScholarGoogle Scholar |
Gremer JR, Kimball HJ, Venable DL (2016) Within- and among-year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment. Ecology Letters 19, 1209–1218.
| Within- and among-year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment.Crossref | GoogleScholarGoogle Scholar |
Gros A, Poethke HJ, Hovestadt T (2006) Evolution of local adaptations in dispersal strategies. Oikos 114, 544–552.
| Evolution of local adaptations in dispersal strategies.Crossref | GoogleScholarGoogle Scholar |
Gross KL (1984) Effects of seed size and growth form on seedling establishment of six monocarpic perennial plants. Journal of Ecology 72, 369–387.
| Effects of seed size and growth form on seedling establishment of six monocarpic perennial plants.Crossref | GoogleScholarGoogle Scholar |
Jakobsson A, Eriksson O (2003) Trade-offs between dispersal and competitive ability: a comparative study of wind-dispersed Asteraceae forbs. Evolutionary Ecology 17, 233–246.
| Trade-offs between dispersal and competitive ability: a comparative study of wind-dispersed Asteraceae forbs.Crossref | GoogleScholarGoogle Scholar |
Jongejans E, Skarpaas O, Tipping PW, Shea K (2007) Establishment and spread of founding populations of an invasive thistle: the role of competition and seed limitation. Biological Invasions 9, 317–325.
| Establishment and spread of founding populations of an invasive thistle: the role of competition and seed limitation.Crossref | GoogleScholarGoogle Scholar |
Jurado E, Westoby M (1992) Seedling growth in relation to seed size among species of arid Australia. Journal of Ecology 80, 407–416.
| Seedling growth in relation to seed size among species of arid Australia.Crossref | GoogleScholarGoogle Scholar |
Leishman MR (2001) Does the seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality. Oikos 93, 294–302.
| Does the seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality.Crossref | GoogleScholarGoogle Scholar |
Lu JJ, Tan DY, Baskin JM, Baskin CC (2013) Trade-offs between seed dispersal and dormancy in an amphi-basicarpic cold desert annual. Annals of Botany 112, 1815–1827.
| Trade-offs between seed dispersal and dormancy in an amphi-basicarpic cold desert annual.Crossref | GoogleScholarGoogle Scholar |
Marchetto KM, Jongejans E, Shea K, Isard SA (2010) Shipment and storage effects on the terminal velocity of seeds. Ecological Research 25, 83–92.
| Shipment and storage effects on the terminal velocity of seeds.Crossref | GoogleScholarGoogle Scholar |
Martorell C, Martinez-Lopez M (2014) Informed dispersal in plants: Heterosperma pinnatum (Asteracease) adjusts its dispersal mode to escape from competition and water stress. Oikos 123, 225–231.
| Informed dispersal in plants: Heterosperma pinnatum (Asteracease) adjusts its dispersal mode to escape from competition and water stress.Crossref | GoogleScholarGoogle Scholar |
Mathias A, Kisdi E, Olivieri I (2001) Divergent evolution of dispersal in a heterogeneous landscape. Evolution 55, 246–259.
| Divergent evolution of dispersal in a heterogeneous landscape.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvlvFKlsA%3D%3D&md5=55ef8e13ae1f5c52d9992102cc166116CAS |
Matlack GR (1987) Diaspore size, shape, and fall behaviour in wind-dispersed plant species. American Journal of Botany 74, 1150–1160.
| Diaspore size, shape, and fall behaviour in wind-dispersed plant species.Crossref | GoogleScholarGoogle Scholar |
Meyer SE, Carlson SL (2001) Achene mass variation in Ericameria nauseosus (Asteraceae) in relation to dispersal ability and seedling fitness. Functional Ecology 15, 274–281.
| Achene mass variation in Ericameria nauseosus (Asteraceae) in relation to dispersal ability and seedling fitness.Crossref | GoogleScholarGoogle Scholar |
Mølgaard P (1977) Competitive effect of grass on establishment and performance of Taraxacum officinale. Oikos 29, 376–382.
| Competitive effect of grass on establishment and performance of Taraxacum officinale.Crossref | GoogleScholarGoogle Scholar |
Monty A, Mahy G (2010) Evolution of dispersal traits along an invasion route in the wind-dispersed Senecio inaequidens (Asteraceae). Oikos 119, 1563–1570.
| Evolution of dispersal traits along an invasion route in the wind-dispersed Senecio inaequidens (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Muller-Landau HC (2010) The tolerance-fecundity trade-off and the maintenance of diversity in seed size. Proceedings of the National Academy of Sciences of the United States of America 107, 4242–4247.
| The tolerance-fecundity trade-off and the maintenance of diversity in seed size.Crossref | GoogleScholarGoogle Scholar |
Niklas KJ (1994) ‘Plant allometry: the scaling of form and process.’ (University of Chicago Press: Chicago, IL, USA)
Picó FX, Ouborg NJ, van Groenendael JM (2003) Fitness traits and dispersal ability in the herb Tragopogon pratensis (Asteraceae): decoupling the role of inbreeding depression and maternal effects. Plant Biology 5, 522–530.
| Fitness traits and dispersal ability in the herb Tragopogon pratensis (Asteraceae): decoupling the role of inbreeding depression and maternal effects.Crossref | GoogleScholarGoogle Scholar |
Picó FX, Ouborg NJ, van Groenendael JM (2004) Influence of selfing and maternal effects on life-cycle traits and dispersal ability in the herb Hypochaeris radicata (Asteraceae). Botanical Journal of the Linnean Society 146, 163–170.
Riba M, Mignot A, Fréville H, Colas B, Imbert E, Vile D, Vivevaire M, Olivieri I (2005) Variation in dispersal traits in a narrow-endemic plant species, Centaura corymbosa Pourret. (Asteraceae). Evolutionary Ecology 19, 241–254.
| Variation in dispersal traits in a narrow-endemic plant species, Centaura corymbosa Pourret. (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Sheldon JC, Burrows FM (1973) The dispersal effectiveness of the achene-pappus units of selected Compositae in steady winds with convection. New Phytologist 72, 665–675.
| The dispersal effectiveness of the achene-pappus units of selected Compositae in steady winds with convection.Crossref | GoogleScholarGoogle Scholar |
Skarpaas O, Silverman EJ, Jongejans E, Shea K (2011) Are the best dispersers the best colonizers? Seed mass, dispersal and establishment in Carduus thistle. Evolutionary Ecology 25, 155–169.
| Are the best dispersers the best colonizers? Seed mass, dispersal and establishment in Carduus thistle.Crossref | GoogleScholarGoogle Scholar |
Soons MB, Heil GW (2002) Reduced colonization capacity in fragmented populations of wind-dispersed grassland forbs. Journal of Ecology 90, 1033–1043.
| Reduced colonization capacity in fragmented populations of wind-dispersed grassland forbs.Crossref | GoogleScholarGoogle Scholar |
Stearns SC (1992) ‘The evolution of life histories.’ (Oxford University Press: Oxford)
Trakhtenbrot A, Nathan R, Perry G, Richardson DM (2005) The importance of long-distance dispersal in biodiversity conservation. Diversity & Distributions 11, 173–181.
| The importance of long-distance dispersal in biodiversity conservation.Crossref | GoogleScholarGoogle Scholar |
Travis JMJ, Dytham C (2002) Dispersal evolution during invasions. Evolutionary Ecology Research 4, 1119–1129.
Turnbull LA, Rees M, Crawley MJ (1999) Seed mass and the competition/colonization trade-off: a sowing experiment. Journal of Ecology 87, 899–912.
| Seed mass and the competition/colonization trade-off: a sowing experiment.Crossref | GoogleScholarGoogle Scholar |
Venable DL (1992) Size-number trade-offs and the variation of seed size with plant resource status. American Naturalist 140, 287–304.
| Size-number trade-offs and the variation of seed size with plant resource status.Crossref | GoogleScholarGoogle Scholar |
Venable DL, Brown JS (1988) The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. American Naturalist 131, 360–384.
| The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments.Crossref | GoogleScholarGoogle Scholar |
Warton DI, Wright IJ, Falster DS (2006) Bivariate line-fitting methods for allometry. Biological Reviews of the Cambridge Philosophical Society 81, 259–291.
| Bivariate line-fitting methods for allometry.Crossref | GoogleScholarGoogle Scholar |
Weiner J (1990) Asymmetric competition in plant populations. Trends in Ecology & Evolution 5, 360–364.
| Asymmetric competition in plant populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7hsVakug%3D%3D&md5=a844678532e90b69cb058f146ec5d477CAS |
Welham CV, Setter RA (1998) Comparison of size-dependant reproductive in two dandelion (Taraxacum officinale) populations. Canadian Journal of Botany 76, 166–173.
| Comparison of size-dependant reproductive in two dandelion (Taraxacum officinale) populations.Crossref | GoogleScholarGoogle Scholar |
Willis CG, Hall JC, de Casas R, Wang TY, Donohue K (2014) Diversification and the evolution of dispersal ability in the tribe Brassicaceae. Annals of Botany 114, 1675–1686.
| Diversification and the evolution of dispersal ability in the tribe Brassicaceae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M3ivFymsw%3D%3D&md5=77fbffe0bb2ed6daba1005411678dfe0CAS |
