Not only size matters: achene morphology affects time of seedling emergence in three heterocarpic species of Anacyclus (Anthemideae, Asteraceae)


  • Rubén Torices Centro de Ecologia Funcional, Universidade de Coimbra
  • Alicia Agudo Real Jardín Botánico, CSIC(RJB-CSIC)
  • Inés Álvarez Real Jardín Botánico, CSIC(RJB-CSIC)



bet-hedging, Compositae, heterocarpy, mixed strategy, position effects, weeds, winged fruits


The production of two or more distinct fruit types by an individual, i.e. heterocarpy, is considered as a mixed dispersal strategy in which a proportion of the offspring is able to colonize new sites, whilst others remain near the maternal location. Here, we aimed to explore the effects of achene morphology (winged vs. unwinged achenes) and achene size –measured here as achene mass– on post-dispersal life-history traits (probability and time of seedling emergence) in three heterocarpic Anacyclus species (Anthemideae, Asteraceae). Morphology, size and germination performance were studied in achenes from six populations of Anacyclus clavatus (Desf.) Pers., A. homogamos (Maire) Humphries, and A. valentinus L. Our results show that achene morphology and size were related to their position within the capitulum, such that outer, winged achenes were significantly heavier than the inner, unwinged ones. Additionally, winged achenes germinated faster than unwinged ones. This pattern may be related to the sequential achene time of release displayed by these species. Finally, our findings cast doubt on the role of wings as structures that favor dispersal by wind in these three species of Anacyclus.


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Aguado, M., Vicente, M.J., Miralles, J., Franco, J.A. & Martínez-Sánchez, J.J. 2012. Aerial seed bank and dispersal traits in Anthemis chrysantha (Asteraceae), a critically endangered species. Flora 207: 275-282.

Anderberg, A.A., Baldwin, B.G., Bayer, R.G., Breitwieser, J., Jeffrey, C., Dioon, M.O., Eldenas, P., Funk, V., Garcia-Jacas. N., Hind, D.J.N., Karis, P.O., Lack, H.W., Nesom, G., Nordenstam, B., Oberpreiler, C., Panero, J.L., Puttock, C., Robinson, H., Stuessy, T.F., Susanna, A., Urtubey, E., Vogt, R., Ward, J. & Watson, L.E. 2007. Compositae. In: Kadereit, J.W. & Jeffrey, C. (eds.), The Families and Genera of Vascular Plants. Volume VIII. Flowering Plants. Eudicots. Asterales: 61-568. Springer. Berlin.

Andersson, S. 1996. Seed size as a determinant of germination rate in Crepis tectorum (Asteraceae): evidence from a seed burial experiment. Canadian Journal of Botany 74: 568-572.

Bastida, F. & Menéndez, J. 2004. Germination requirements and disperal timing in two heterocarpic weedy Asteraceae. Communications in Agricultural and Applied Biological Sciences 69: 67-76. PMid:15759397

Bastida, F., González-Andújar, J.L., Monteagudo, F.J. & Menéndez, J. 2010. Aerial seed bank dynamics and seedling emergence patterns in two annual Mediterranean Asteraceae. Journal of Vegetation Science 21: 541-550.

Bello, M.A., Álvarez, I., Torices, R., Fuertes-Aguilar, J. 2013. Floral development and evolution of capitulum structure in Anacyclus (Anthemideae, Asteraceae). Annals of Botany (doi:10.1093/aob/mcs301).

Benard R.B., Toft C.A. 2007. Effect of seed size on seedling performance in a long lived desert perennial shrub (Ericameria nauseosa: Asteraceae). International Journal of Plant Sciences 168: 1027-1033.

Brändel, M. 2004. Dormancy and germination of heteromorphic achenes of Bidens frondosa. Flora 233: 228-233.

Brändel, M. 2007. Ecology of achene dimorphism in Leontodon saxatilis. Annals of Botany 100: 1189-1197. PMid:17901060 PMCid:PMC2759255

Cousan, R., Dytham, C. & Law, R. 2008. Dispersal in Plants. A population persepective. Oxford University Press. New York

Dubois, J. & Cheptou, P.-O. 2012. Competition/colonization syndrome mediated by early germination in non-dispersing achenes in the heteromorphic species Crepis sancta. Annals of Botany 110: 1245-1251 PMid:23022677

Filho, S.P.R.M. & Takaki, M. 2011. Dimorphic cypsela germination and plant growth in Synedrella nodiflora (L.) Gaertn. (Asteraceae). Brazilian Journal of Biology 71: 541-548.

Fumanal, B., Chauvel, B., Sabatier, A. & Bretagnolle, F. 2007. Variability and cryptic heteromorphism of Ambrosia artemisiifolia seeds: what consequences for its invasion in France? Annals of Botany 100: 305-13. PMid:17575284 PMCid:PMC2735321

Gadgil, M. 1971. Dispersal: population consequences and evolution. Ecology 52: 253-260.

Gillespie, J.H. 1977. Natural selection for variance in offspring numbers: a new evolutionary principle. American Naturalist 111: 1010-1014.

Gutterman, Y. 1994. Strategies of seed dispersal and germination in plants inhabiting deserts. The Botanical Review 60: 373-425.

Gutterman Y. & Ginott, S. 1994. Long-term protected "seed bank" in dry inflorescences of Asteriscus pygmaeus; achene dispersal mechanism and germination. Journal of Arid Environments 26: 149-163.

Harper, J.L. 1977. Population biology of plants. Academic Press. Toronto.

Herrera, C.M. 2009. Multiplicity in Unity: plant subindividual variation and interactions with animals. The University of Chicago Press. London.

Humphries, C.J. 1979. A revision of the genus Anacyclus L. (Compositae: Anthemideae). Bulletin of the British Museum (Natural History) 7: 83-142.

Imbert, E. 2002. Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology Evolution and Systematics 5: 13-36.

Imbert, E., Escarré J. & Lepart J. 1996. Achene dimorphism and amongpopulation variation in Crepis sancta (Asteraceae). International Journal of Plant Sciences 157: 309-315.

Imbert, E. & Ronce, O. 2001. Phenotypic plasticity for dispersal ability in the seed heteromorphic Crepis sancta (Asteraceae). Oikos 93: 126-134. Koller, D. & Roth, N. 1964. Studies of the ecological and physiological significance of amphicarpy in Gymnarrhena micrantha (Compositae). American Journal of Botany 51: 26-35.

Levin, S.A., Cohen, D. & Hastings A. 1984. Dispersal strategies in patchy environments. Theoretical Population Biology 26: 165-191

Lu, J., Tan, D., Baskin, J.M. & Baskin, C.C. 2010. Fruit and seed heteromorphism in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and possible adaptive significance. Annals of Botany 105: 999-1014. PMid:20348559 PMCid:PMC2876001

Manchester, S.R. & O'Leary, E.L. 2010. Phylogenetic distribution and identification of fin-winged fruits. The Botanical Review 76: 1-82.

Mandák, B. 1997. Seed heteromorphism and the life cycle of plants: a literature review. Preslia 69: 129-159.

Maxwell, C.D., Zobel, A. & Woodfine, D. 1994. Somatic polymorphism in the achenes of Tragopogon dubius. Canadian Journal of Botany 72: 1282-1288.

McEvoy, P.B. 1984. Dormancy and dispersal in dimorphic achenes of tansy ragwort. Oecologia 61: 160-168.

McGinley, M.A. 1989 Within and among plant variation in seed mass and pappus size in Tragopogon dubious. Canadian Journal of Botany 67: 1298-1304.

Meyer, S.E. & Carlson, S.L. 2001. Achene mass variation in Ericameria nauseosus (Asteraceae) in relation to dispersal ability and seedling fitness. Functional Ecology 15: 274-281.

Orrock, J.L. & Christopher, C.C. 2010. Density of intraspecific competitors determines the occurrence and benefits of accelerated germination. American Journal of Botany 97: 694-9. PMid:21622431

Pandey, H.N. & Dubey, S.K. 1988. Achene germination of Parthenium hysterophorus L.: effects of light, temperature, provenance and achene size. Weed Research 28: 185-190.

Parolin, P. 2006. Ombrohydrochory: Rain-operated seed dispersal in plants – With special regard to jet-action dispersal in Aizoaceae. Flora 201: 511-518.

Patterson, H.D. & Thompson, R. 1971. Recovery of inter-block information when block sizes are unequal. Biometrica 58: 545-554

Peters, E.M., Martorell, C. & Ezcurra, E. 2009. The adaptive value of cued seed dispersal in desert plants: Seed retention and release in Mammillaria pectinifera (Cactaceae), a small globose cactus. American Journal of Botany 96: 537-41. PMid:21628209

Porras, R. & Mu-oz, J.M. 2000. Achene heteromorphism in the cleistogamous species Centaurea melitensis. Acta Oecologica 21: 231-243.

Prinzie, T.P. & Chmielewski, J.G. 1994. Significance of achene characteristics and withinachene resource allocation in the germination strategy of tetraploid Aster pilosus var. pilosus (Asteraceae). American Journal of Botany 81: 259-264.

Rai, J.P.N. & Tripathi, R.S. 1982. Adaptive significance of seed reserves in ray achenes of Galinsoga parviflora. Experientia 38: 804-806.

Redbo-Torstensson, P. & Telenius, A. 1995. Primary and secondary seed dispersal by wind and water in Spergularia salina. Ecography 18: 230-237.

Rocha, O.J. 1996. The effects of achene heteromorphism on the dispersal capacity of Bidens pilosa L. International Journal of Plant Sciences 157: 316-322.

Ruiz de Clavijo, E. 1995. The ecological significance of fruit heteromorphism in the amphicarpic species Catananche lutea (Asteraceae). International Journal of Plant Sciences 156: 824-833.

Ruiz de Clavijo, E. 2005. The reproductive strategies of the heterocarpic annual Calendula arvensis (Asteraceae). Acta Oecologica 28: 119-126.

Ruiz de Clavijo, E. & Jiménez, M.J. 1998. The influence of achene type and plant density on growth and biomass allocation in the heterocarpic annual Catananche lutea (Asteraceae). International Journal of Plant Sciences 159: 637-647.

Schoen, D.J. & Lloyd, D.G. 1984. The selection of cleistogamy and heteromorphic diaspores. Biological Journal of the Linnean Society 23: 303-322.

Simons, A.M. 2011. Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proceedings of the Royal Society B 278: 1601-1609. PMid:21411456 PMCid:PMC3081777

Sun, H.Z., Lu, J.J., Tan, D.Y., Baskin, J.M. & Baskin, C.C. 2009. Dormancy and germination characteristics of the trimorphic achenes of Garhadiolus papposus (Asteraceae), an annual ephemeral from the Junggar Desert, China. South African Journal of Botany 75: 537-545.

Tackenberg, O., Poschlod, P. & Bonn, S. 2003. Assessment of wind dispersal potential in plant species. Ecological Monographs 73: 191-205.[0191:AOWDPI]2.0.CO;2

Tanowitz, B.D., Salopek, P.F. & Mahall, B.E. 1987. Differential germination of ray and disc achenes in Hemizonia increscens (Asteraceae). American Journal of Botany 74: 303-312.

Telenius, A. & Torstensson, P. 1989. The seed dimorphism of Spergularia marina in relation to dispersal by wind and water. Oecologia 80: 206-210.

Thomson, F.J., Moles, A.T., Auld, T.D. & Kingsford, R.T. 2011. Seed dispersal distance is more strongly correlated with plant height than with seed mass. Journal of Ecology 99: 1299-1307.

Tielbörger, K., Petruů, M., Lampei, C. 2012. Bet-hedging germination in annual plants: a sound empirical test of the theoretical foundations. Oikos 121: 1860-1868.

Torices, R. & Méndez, M. 2010. Fruit size decline from the margin to the center of capitula is the result of resource competition and architectural constraints. Oecologia 164: 949-958. PMid:20623142

Van der Pijl, L. 1982. Principles of Dispersal in Higher Plant. Springer-Verlag. New York.

Van Mölken, T., Jorritsma-Wienk, L.D., van Hoek, P.H.W. & de Kroon, H. 2005. Only seed size matters for germination in different populations of the dimorphic Tragopogon pratensis subsp. pratensis (Asteraceae). American Journal of Botany 92: 432-7. PMid:21652419

Venable, D.L. 1985. Ecology of achene dimorphism in Heterotheca latifolia. III. Consequences of varied water availability. Journal of Ecology 73: 757-763.

Venable, D.L. 2007. Bet hedging in a guild of desert annuals. Ecology 88: 1086-90. PMid:17536393

Venable, D.L. & Brown J.S. 1993. The population-dynamic functions of seed dispersal. Vegetatio 107/108: 31-55.

Venable, D.L., Búrquez, A., Corral, G., Morales, E. & Espinosa, F. 1987. The ecology of seed heteromorphism in Heterosperma pinnatum in Central Mexico. Ecology 68: 65-76.

Verbeke, G. & Molenberghs, G. 1997. Linear mixed models in practice. A SAS-oriented approach. Springer-Verlag. New York.

Zohary, M. 1950. Evolutionary trends in the fruiting head of Compositae. Evolution 4: 103-109.




How to Cite

Torices, R., Agudo, A., & Álvarez, I. (2013). Not only size matters: achene morphology affects time of seedling emergence in three heterocarpic species of Anacyclus (Anthemideae, Asteraceae). Anales Del Jardín Botánico De Madrid, 70(1), 48–55.