Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-11T09:41:38.915Z Has data issue: false hasContentIssue false

Will the sleeping beauties wake up? Seasonal dormancy cycles in seeds of the holoparasite Cuscuta epithymum

Published online by Cambridge University Press:  19 November 2009

Klaar Meulebrouck*
Affiliation:
Division of Forest, Nature and Landscape, University of Leuven, Celestijnenlaan 200E, B-3001Leuven, Belgium Laboratory of Forestry, Ghent University, Geraardsbergse Steenweg 267, B-9090Melle-Gontrode, Belgium
Kris Verheyen
Affiliation:
Laboratory of Forestry, Ghent University, Geraardsbergse Steenweg 267, B-9090Melle-Gontrode, Belgium
Martin Hermy
Affiliation:
Division of Forest, Nature and Landscape, University of Leuven, Celestijnenlaan 200E, B-3001Leuven, Belgium
Carol Baskin
Affiliation:
Department of Biology, University of Kentucky Lexington, Kentucky405060-055, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky40546-0321, USA
*
*Correspondence Fax: +32 16 32 97 60 Email: klaar.meulebrouck@lne.vlaanderen.be

Abstract

Seed banks are often crucial for the survival of plant species, especially short-lived ones. Nevertheless, empirical studies about the fate of seeds under natural conditions are scarce, particularly for parasitic plants. Therefore, fresh seeds of the holoparasitic Cuscuta epithymum were buried in the field under natural conditions in Belgium or kept at room temperature for up to 31 months, and germination was tested periodically by incubating seeds in light at 23°C. Buried C. epithymum seeds had cyclic changes in their germinability, while those stored dry at room temperature never germinated without scarification. Buried seeds exhibited a seasonal cycle of physiological dormancy, the first to be reported for a species with combinational (i.e. physical+physiological) dormancy. The physiological dormancy of the embryo was broken during winter ( ≤ 5°C) but induced during exposure to late spring temperatures (>10°C). Therefore, germination of C. epithymum seeds is fine tuned to seasonal temperature changes. Each year only a portion of the viable seeds could germinate. The portion of seeds buried in the soil that remained available for delayed germination, i.e. in the seed bank, decreased rather quickly, with only 8.5% of them being viable after 31 months of burial; all seeds stored in the laboratory remained viable. Nonetheless, we concluded that some C. epithymum seeds are capable of surviving for several years in the soil. These data indicate that the parasite is well adapted to survive in a dynamic heathland landscape where conditions for survival change constantly, but it is still sensitive to local extinction.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bakker, J.P., Poschlod, P., Strykstra, R.J., Bekker, R.M. and Thompson, K. (1996) Seed banks and seed dispersal: important topics in restoration ecology. Acta Botanica Neerland 45, 461490.CrossRefGoogle Scholar
Baskin, C.C. and Baskin, J.M. (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Baskin, J.M. and Baskin, C.C. (1985) The annual dormancy cycle in buried weed seeds: a continuum. BioScience 35, 492498.CrossRefGoogle Scholar
Benvenuti, S., Dinelli, G., Bonetti, A. and Catizone, P. (2005) Germination ecology, emergence and host detection in Cuscuta campestris. Weed Research 45, 270278.CrossRefGoogle Scholar
Bouwmeester, H.J. and Karssen, C.M. (1993) Annual changes in dormancy and germination in seeds of Sisymbrium officinale (L.) Scop. The New Phytologist 124, 179191.CrossRefGoogle Scholar
Cheffings, C.M., Farrell, L., Dines, T.D., Jones, R.A., Leack, S.J., McKean, D.R., Pearman, D.A., Preston, C.D., Rumsey, F.J. and Taylor, I. (2005) The vascular plant Red Data List for Great Britain. Species status 7. 1-116. Peterborough, Joint Nature Conservation Committee.Google Scholar
Doyle, G.J. (1993) Cuscuta epithymum (L.) L. (Convolvulaceae), its hosts and associated vegetation in a limestone pavement habitat in the burren lowlands in County Clare (H9), Western Ireland. Biology and environment: Proceedings of the Royal Irish Academy 93B, 6167.Google Scholar
Fenner, M. (2000) Seeds: the ecology of regeneration in plant communities. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Fisher, M. and Matthies, D. (1998) Experimental demography of the rare Gentianella germanica: seed bank formation and microsite effects on seedling establishment. Ecography 21, 269278.CrossRefGoogle Scholar
Gimingham, C.H., Chapman, S.B. and Webb, N.R. (1979) European heathlands. pp. 365413in Goodall, D.W.; Specht, R.L. (Eds) Heathlands and related shrublands: descriptive studies. Amsterdam, Elsevier.Google Scholar
Grime, J.P. (1981) The role of seed dormancy in vegetation dynamics. Annuals of Applied Biology 98, 555558.CrossRefGoogle Scholar
Grundy, A.C., Mead, A. and Burston, S. (2003) Modelling the emergence response of weed seeds to burial depth: interactions with seed density, weight and shape. Journal of Applied Ecology 40, 757770.CrossRefGoogle Scholar
Jayasuriya, K.M.G.G., Baskin, J.M. and Baskin, C.C. (2008a) Cycling of sensitivity to physical dormancy-break in seeds of Ipomoea lacunosa (Convolvulaceae) and ecological significance. Annals of Botany 101, 341352.CrossRefGoogle ScholarPubMed
Jayasuriya, K.M.G.G., Baskin, J.M., Geneve, R.L., Baskin, C.C. and Chien, C. (2008b) Physical dormancy in seeds of the holoparasitic angiosperm Cuscuta australis (Convolvulaceae, Cuscutaceae): dormancy-breaking requirements, anatomy of the water gap and sensitivity cycling. Annals of Botany 102, 3948.CrossRefGoogle Scholar
Jayasuriya, K.M.G.G., Baskin, J.M. and Baskin, C.C. (2009) Sensitivity cycling and its ecological role in seeds with physical dormancy. Seed Science Research 19, 313.CrossRefGoogle Scholar
Kleyer, M., Biedermann, R., Henle, K., Obermaier, E., Poethke, H., Poschlod, P., Schröder, B., Settele, J. and Vetterlein, D. (2007) Mosaic cycles in agricultural landscapes of Northwest Europe. Basic and Applied Ecology 8, 295309.CrossRefGoogle Scholar
Klinkhamer, P.G.L., De Jong, T.J. and Van der Meijden, E. (1998) Production, dispersal and predation of seeds in the biennial Cirsium vulgare. Journal of Ecology 76, 403414.CrossRefGoogle Scholar
López-Granados, F. and Garcia-Torres, L. (1999) Longevity of crenate broomrape (Orobanche crenata) seed under soil and laboratory conditions. Weed Science 47, 161166.CrossRefGoogle Scholar
Matusova, R., Rani, K., Verstappen, F.W.A., Franssen, M.C.R., Beale, M.H. and Bouwmeester, H.J. (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiology 139, 920934.CrossRefGoogle ScholarPubMed
Meulebrouck, K., Ameloot, E., Verheyen, K. and Hermy, M. (2007) Local and regional factors affecting the distribution of the endangered holoparasite Cuscuta epithymum in heathlands. Biological Conservation 140, 818.CrossRefGoogle Scholar
Meulebrouck, K., Ameloot, E., Van Assche, J.A., Verheyen, K., Hermy, M. and Baskin, C.C. (2008) Germination ecology of the holoparasite Cuscuta epithymum. Seed Science Research 18, 2534.CrossRefGoogle Scholar
Meulebrouck, K., Ameloot, E., Brys, R., Tanghe, L., Verheyen, K. and Hermy, M. (2009a) Hidden in the host – unexpected vegetation hibernation of the holoparasite Cuscuta epithymum (L.) L. and its implications for population persistence. Flora 204, 306315.CrossRefGoogle Scholar
Meulebrouck, K., Verheyen, K., Brys, R. and Hermy, M. (2009b) Limited by the host: host age hampers establishment of holoparasite Cuscuta epithymum. Acta Oecologica 35, 533540.CrossRefGoogle Scholar
Meyer, S.E., Quinney, D. and Weaver, J. (2006) A stochastic population model for Lepidium papilliferum (Brassicaceae), a rare desert ephemeral with a persistent seed bank. American Journal of Botany 93, 891902.CrossRefGoogle ScholarPubMed
Piessens, K., Honnay, O. and Hermy, M. (2005) The role of fragment area and isolation in the conservation of heathland species. Biological Conservation 122, 6169.CrossRefGoogle Scholar
Pons, T.L. (1991) Dormancy, germination and mortality of seeds in a chalk-grassland flora. Journal of Ecology 79, 765780.CrossRefGoogle Scholar
Russi, L., Cocks, P.S. and Roberts, E.H. (1992) Seed bank dynamics in a Mediterranean grassland. Journal of Applied Ecology 29, 763771.CrossRefGoogle Scholar
Schaminée, J.H.J., Stortelder, A.H.F. and Weeda, E.J. (1996) De vegetatie van Nederland: deel 3. Plantengemeenschappen van graslanden, zomen en droge heiden. Leiden, Opulus Press.Google Scholar
Valleriani, A. (2006) Evolutionarily stable germination strategies with time-correlated yield. Theoretical Population Biology 71, 255261.CrossRefGoogle Scholar
Van Assche, J.A. and Vanlerberghe, K.A. (1989) The role of temperature on the dormancy cycle of seeds of Rumex obtusifolius L. Functional Ecology 3, 107115.CrossRefGoogle Scholar
Van Assche, J.A., Debucquoy, K.L.A. and Rommens, W.A.F. (2003) Seasonal cycle in the germination capacity of buried seeds of some Leguminosae (Fabaceae). The New Phytologist 158, 315323.CrossRefGoogle Scholar
Van Landuyt, W., Hoste, I., Vanhecke, L., Van den Bremt, P., Vercruysse, W. and De Beer, D. (2006) Atlas van de Flora van Vlaanderen en het Brussels Gewest. België, Instituut voor natuur- en bosonderzoek, National Botanic Garden of Belgium and FLo.Wer.Google Scholar
Venable, D.L. and Lawlor, L. (1980) Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46, 272282.CrossRefGoogle ScholarPubMed
Venable, D.L. and Brown, J.S. (1988) The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. The American Naturalist 131, 360384.CrossRefGoogle Scholar
Webb, N.R. (1998) The traditional management of European heathlands. Journal of Applied Ecology 35, 987990.CrossRefGoogle Scholar
Weeda, E.J., Westra, R., Westra, Ch. and Westra, T. (1988) Warkruidfamilie (Cuscutaceae). pp. 115118in Weeda, E.J.Westra, R.Westra, Ch.Westra, T. (Eds) Nederlandse Oecologische Flora. Wilde planten en hun relaties, Vol. 3, Amsterdam, IVN.Google Scholar