Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-19T11:29:05.919Z Has data issue: false hasContentIssue false

Seed-coat thickness data clarify seed size–seed-bank persistence trade-offs in Abutilon theophrasti (Malvaceae)

Published online by Cambridge University Press:  09 May 2014

Brian J. Schutte*
Affiliation:
US Department of Agriculture, Agricultural Research Service, Global Change and Photosynthesis Research Unit, 1201 West Gregory Drive, Urbana, Illinois 61801, USA
Adam S. Davis
Affiliation:
US Department of Agriculture, Agricultural Research Service, Global Change and Photosynthesis Research Unit, 1201 West Gregory Drive, Urbana, Illinois 61801, USA
Stephen A. Peinado Jr
Affiliation:
Department of Entomology, Plant Pathology and Weed Science, New Mexico State University, MSC 3BE, Las Cruces, NM 88003-8003, USA
Jamshid Ashigh
Affiliation:
Department of Entomology, Plant Pathology and Weed Science, New Mexico State University, MSC 3BE, Las Cruces, NM 88003-8003, USA
*
*Correspondence Email: [email protected]

Abstract

Theoretical models predict that seed size and seed-bank persistence evolve interdependently, such that strong selection for one trait corresponds with weak selection for the other. This framework has been supported and rejected by empirical data, and thus, conclusive evidence is lacking. We expanded the seed size–persistence framework to include seed-coat thickness, a defence trait previously correlated with seed survival in soil. To do this, we used Abutilon theophrasti accessions with varied evolutionary histories and we quantified associations among seed traits including morphology, size, coat thickness, dormancy (percentage of viable seeds that fail to germinate under optimum conditions) and seed-bank persistence (percentage of viable seeds remaining after 1 year of burial). Statistical models were developed to test the hypothesis that combined measurements of seed-coat thickness and seed size better explain variability in seed-bank persistence than seed-size data alone. Results indicated that measurements of seed size (length, width, mass) were negatively correlated with coat:width ratio (coat thickness relative to seed width) and coat:mass ratio (coat thickness relative to seed mass). Accessions characterized by smaller seeds with proportionally thicker seed coats were more dormant and more persistent in soil than accessions characterized by larger seeds with proportionally thinner seed coats. Seed-coat thickness data improved the explanatory power of logistic regression models for seed-size effects on both seed-bank persistence and dormancy. These results indicate that supplementing seed-size data with seed-defence data may clarify previously reported contradictory results regarding trade-offs between seed size and seed-bank persistence.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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

Alexander, H.M., Pilson, D., Moody-Weis, J. and Slade, N.A. (2009) Geographic variation in dynamics of an annual plant with a seed bank. Journal of Ecology 97, 13901400.Google Scholar
Andersen, R.N. (1988) Outcrossing in velvetleaf (Abutilon theophrasti). Weed Science 36, 599602.Google Scholar
Baloch, H.A., DiTommaso, A. and Watson, A.K. (2001) Intrapopulation variation in Abutilon theophrasti seed mass and its relationship to seed germinability. Seed Science Research 11, 335343.Google Scholar
Banko, P.C., Cipollini, M.L., Breton, G.W., Paulk, E., Wink, M. and Izhaki, I. (2002) Seed chemistry of Sophora chrysophylla (mamane) in relation to diet of specialist avian seed predator Loxioides bailleui (palila) in Hawaii. Journal of Chemical Ecology 28, 13931410.Google Scholar
Baskin, C.C. and Baskin, J.M. (1998) Seeds: Ecology, biogeography, and evolution of dormancy and germination. San Diego, California, USA, Academic Press.Google Scholar
Brainard, D.C., DiTommaso, A. and Mohler, C.L. (2007) Intraspecific variation in seed characteristics of Powell amaranth (Amaranthus powellii) from habitats with contrasting crop rotation histories. Weed Science 55, 218226.Google Scholar
Burnham, K.P. and Anderson, D.R. (2002) Model selection and inference: A practical information–theoretic approach (2nd edition). New York, Springer Verlag.Google Scholar
Cardina, J. and Norquay, H.M. (1997) Seed production and seedbank dynamics in subthreshold velvetleaf (Abutilon theophrasti) populations. Weed Science 45, 8590.Google Scholar
Cerabolini, B., Ceriani, R.M., Caccianiga, M., Andreis, R.D. and Raimondi, B. (2003) Seed size, shape and persistence in soil: a test on Italian flora from Alps to Mediterranean coasts. Seed Science Research 13, 7585.CrossRefGoogle Scholar
Childs, D.Z., Metcalf, C.J.E. and Rees, M. (2010) Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants. Proceedings of the Royal Society B – Biological Sciences 277, 30553064.Google Scholar
Cohen, D. (1966) Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology 12, 119129.Google Scholar
Comins, H.N., Hamilton, W.D. and May, R.M. (1980) Evolutionarily stable dispersal strategies. Journal of Theoretical Biology 82, 205230.Google Scholar
Corbineau, F. (2012) Markers of seed quality: from present to future. Seed Science Research 22, S61S68.CrossRefGoogle Scholar
Dalling, J.W., Davis, A.S., Schutte, B.J. and Arnold, A.E. (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99, 8995.Google Scholar
Davis, A.S., Cardina, J., Forcella, F., Johnson, G.A., Kegode, G., Lindquist, J.L., Lusche, E.C., Renner, K.A., Sprague, C.L. and Williams, M.M. (2005) Environmental factors affecting seed persistence of annual weeds across the US corn belt. Weed Science 53, 860868.Google Scholar
Davis, A.S., Schutte, B.J., Iannuzzi, J. and Renner, K.A. (2008) Chemical and physical defense of weed seeds in relation to soil seedbank persistence. Weed Science 56, 676684.Google Scholar
de Jong, T.J., Isanta, M.T. and Hesse, E. (2013) Comparison of the crop species Brassica napus and wild B. rapa: characteristics relevant for building up a persistent seed bank in the soil. Seed Science Research 23, 169179.Google Scholar
England, P.R., Whelan, R.J. and Ayre, D.J. (2003) Effects of seed bank disturbance on the fine-scale genetic structure of populations of the rare shrub Grevillea macleayana . Heredity 91, 475480.Google Scholar
Fenner, M. and Thompson, K. (2005) The ecology of seeds. Cambridge UK, Cambridge University Press.Google Scholar
Funes, G., Basconcelo, S., Diaz, S. and Cabido, M. (1999) Seed size and shape are good predictors of seed persistence in soil in temperate mountain grasslands of Argentina. Seed Science Research 9, 341345.CrossRefGoogle Scholar
Gardarin, A., Durr, C., Mannino, M.R., Busset, H. and Colbach, N. (2010) Seed mortality in the soil is related to seed coat thickness. Seed Science Research 20, 243256.CrossRefGoogle Scholar
Godwin, I.D., Aitken, E.A.B. and Smith, L.W. (1997) Application of inter simple sequence repeat (ISSR) markers to plant genetics. Electrophoresis 18, 15241528.Google Scholar
Goggin, D.E., Powles, S.B. and Steadman, K.J. (2011) Selection for low or high primary dormancy in Lolium rigidum Gaud seeds results in constitutive differences in stress protein expression and peroxidase activity. Journal of Experimental Botany 62, 10371047.Google Scholar
Gross, K.L. (1984) Effects of seed size and growth form on seedling establishment of 6 monocarpic perennial plants. Journal of Ecology 72, 369387.Google Scholar
Johnson, D.E. (1998) Applied multivariate methods for data analysts. Pacific Grove, California, USA, Duxbury Press.Google Scholar
Khan, M., Cavers, P.B., Kane, M. and Thompson, K. (1997) Role of the pigmented seed coat of proso millet (Panicum miliaceum L.) in imbibition, germination and seed persistence. Seed Science Research 7, 2125.Google Scholar
Kremer, R.J. (1986) Antimicrobial activity of velvetleaf (Abutilon theophrasti) seeds. Weed Science 34, 617622.Google Scholar
Kremer, R.J., Hughes, L.B. and Aldrich, R.J. (1984) Examination of microorganisms and deterioration resistance mechanisms associated with velvetleaf seed. Agronomy Journal 76, 745749.Google Scholar
Kurokawa, S., Shimizu, N., Uozumi, S. and Yoshimura, Y. (2003) ISSR variation in a worldwide collection of velvetleaf (Abutilon theophrasti) and the genetic background of weedy strains mingled in grains imported into Japan. Weed Biology and Management 3, 179183.CrossRefGoogle Scholar
LaCroix, L.J. and Staniforth, D.W. (1964) Seed dormancy in velvetleaf. Weeds 12, 171174.Google Scholar
Leishman, M.R. and Westoby, M. (1998) Seed size and shape are not related to persistence in soil in Australia in the same way as in Britain. Functional Ecology 12, 480485.Google Scholar
McDonald, M.B. (1999) Seed deterioration: physiology, repair and assessment. Seed Science and Technology 27, 177237.Google Scholar
Medovic, A. and Horvath, F. (2012) Content of a storage jar from the Late Neolithic site of HdmezAvasarhely-Gorzsa, south Hungary: a thousand carbonized seeds of Abutilon theophrasti Medic. Vegetation History and Archaeobotany 21, 215220.Google Scholar
Michaels, H.J., Benner, B., Hartgerink, A.P., Lee, T.D., Rice, S., Willson, M.F. and Bertin, R.I. (1988) Seed size variation: magnitude, distribution, and ecological correlates. Evolutionary Ecology 2, 157166.Google Scholar
Moegenburg, S.M. (1996) Sabal palmetto seed size: causes of variation, choices of predators, and consequences for seedlings. Oecologia 106, 539543.Google Scholar
Mohamedyasseen, Y., Barringer, S.A., Splittstoesser, W.E. and Costanza, S. (1994) The role of seed coats in seed viability. Botanical Review 60, 426439.Google Scholar
Moles, A.T. and Leishman, M.R. (2008) The seedling as part of a plant's life history strategy. pp. 217238 in Leck, M.A.; Parker, V.T; Simpson, R.L. (Eds) Seedling ecology and evolution. Cambridge, UK, Cambridge University Press.Google Scholar
Moles, A.T., Hodson, D.W. and Webb, C.J. (2000) Seed size and shape and persistence in the soil in the New Zealand flora. Oikos 89, 541545.Google Scholar
Nurse, R.E. and DiTommaso, A. (2005) Corn competition alters the germinability of velvetleaf (Abutilon theophrasti) seeds. Weed Science 53, 479488.Google Scholar
Paulsen, T.R., Colville, L., Kranner, I., Daws, M.I., Hogstedt, G., Vandvik, V. and Thompson, K. (2013) Physical dormancy in seeds: a game of hide and seek? New Phytologist 198, 496503.Google Scholar
Peco, B., Traba, J., Levassor, C., Sanchez, A.M. and Azcarate, F.M. (2003) Seed size, shape and persistence in dry Mediterranean grass and scrublands. Seed Science Research 13, 8795.Google Scholar
Peters, J. (2000) Tetrazolium testing handbook. Contribution No. 29 to the Handbook on Seed Testing. Lincoln, Nebraska, USA, Association of Official Seed Analysts.Google Scholar
Rasband, W.S. (2007) ImageJ. Bethesda, Maryland, USA, US National Institutes of Health.Google Scholar
Rees, M. (1996) Evolutionary ecology of seed dormancy and seed size. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 351, 12991308.Google Scholar
Rohlf, F.J. (1997) NTSYS-PC 2.02. Numerical taxonomy and multivariate analysis system. Setauket, New York, Exeter Software.Google Scholar
Saatkamp, A., Affre, L., Dutoit, T. and Poschlod, P. (2009) The seed bank longevity index revisited: limited reliability evident from a burial experiment and database analyses. Annals of Botany 104, 715724.Google Scholar
Schutte, B.J., Davis, A.S., Renner, K.A. and Cardina, J. (2008a) Maternal and burial environment effects on seed mortality of velvetleaf (Abutilon theophrasti) and giant foxtail (Setaria faberi). Weed Science 56, 834840.Google Scholar
Schutte, B.J., Regnier, E.E. and Harrison, S.K. (2008b) The association between seed size and seed longevity among maternal families in Ambrosia trifida L. populations. Seed Science Research 18, 201211.Google Scholar
Sork, V.L. and Smouse, P.E. (2006) Genetic analysis of landscape connectivity in tree populations. Landscape Ecology 21, 821836.Google Scholar
Sosnoskie, L.M. (2005) Investigations in weed biology: studies at the plant, population, and community levels. PhD thesis, The Ohio State University, Columbus, OH, USA. Google Scholar
Spencer, N.R. (1984) Velvetleaf, Abutilon theophrasti (Malvaceae), history and economic impact in the United States. Economic Botany 38, 407416.Google Scholar
Stanton, M.L. (1985) Seed size and emergence time within a stand of wild radish (Raphanus raphanistrum L.): the establishment of a fitness hierarchy. Oecologia 67, 524531.Google Scholar
Thompson, K., Band, S.R. and Hodgson, J.G. (1993) Seed size and shape predict persistence in soil. Functional Ecology 7, 236241.Google Scholar
Thompson, K., Bakker, J.P., Bekker, R.M. and Hodgson, J.G. (1998) Ecological correlates of seed persistence in soil in the north-west European flora. Journal of Ecology 86, 163169.Google Scholar
Thompson, K., Jalili, A., Hodgson, J.G., Hamzeh'ee, B., Asri, Y., Shaw, S., Shirvany, A., Yazdani, S., Khoshnevis, M., Zarrinkamar, F., Ghahramani, M.A. and Safavi, R. (2001) Seed size, shape and persistence in the soil in an Iranian flora. Seed Science Research 11, 345355.Google Scholar
Van der Wall, S.B. (1998) Foraging success of granivorous rodents: Effects of variation in seed and soil water on olfaction. Ecology 79, 233241.Google Scholar
Vaughton, G. and Ramsey, M. (1998) Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). Journal of Ecology 86, 563573.Google Scholar
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. American Naturalist 131, 360384.Google Scholar
Venable, D.L. and Lawlor, L. (1980) Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46, 272282.Google Scholar
Wang, N., Jiao, J.Y., Jia, Y.F. and Wang, D.L. (2011) Seed persistence in the soil on eroded slopes in the hilly-gullied Loess Plateau region, China. Seed Science Research 21, 295304.CrossRefGoogle Scholar
Warwick, S.I. and Black, L.D. (1986) Geneological variation in recently established populations of Abutilon theophrasti (velvetleaf). Canadian Journal of Botany 64, 16321643.Google Scholar
Warwick, S.I. and Black, L.D. (1988) The biology of Canadian weeds. 90. Abutilon theophrasti . Canadian Journal of Plant Science 68, 10691085.Google Scholar
Wiles, L.J., Barlin, D.H., Schweizer, E.E., Duke, H.R. and Whitt, D.E. (1996) A new soil sampler and elutriator for collecting and extracting weed seeds from soil. Weed Technology 10, 3541.Google Scholar
Winn, A.A. (1985) Effects of seed size and microsite on seedling emergence of Prunella vulgaris in four habitats. Journal of Ecology 73, 831840.Google Scholar
Winn, A.A. (1991) Proximate and ultimate sources of within-individual variation in seed mass in Prunella vulgaris (Lamiaceae). American Journal of Botany 78, 838844.Google Scholar
Xu, C.M., Zhang, Y.L., Wang, J. and Lu, J.A. (2010) Extraction, distribution and characterisation of phenolic compounds and oil in grapeseeds. Food Chemistry 122, 688694.Google Scholar
Yu, S.L., Sternberg, M., Kutiel, P. and Chen, H.W. (2007) Seed mass, shape, and persistence in the soil seed bank of Israeli coastal sand dune flora. Evolutionary Ecology Research 9, 325340.Google Scholar
Zas, R., Cendan, C. and Sampedro, L. (2013) Mediation of seed provisioning in the transmission of environmental maternal effects in Maritime pine (Pinus pinaster Aiton). Heredity 111, 248255.Google Scholar
Zhang, J.H. and Hamill, A.S. (1997) Seed weight, intraspecific competition, and plant performance in Abutilon theophrasti . Canadian Journal of Botany 75, 16141620.Google Scholar
Zhao, L.P., Wu, G.L. and Cheng, J.M. (2011) Seed mass and shape are related to persistence in a sandy soil in northern China. Seed Science Research 21, 4753.Google Scholar
Zuur, A.F., Ieno, E.N. and Elphick, C.S. (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 314.CrossRefGoogle Scholar