In largely clonal plants, splitting of a maternal plant into potentially independent plants (ramets) is usually spontaneous; however, such fragmentation also occurs in otherwise non-clonal species due to application of external force. This process might play an important yet largely overlooked role for otherwise non-clonal plants by providing a mechanism to regenerate after disturbance. Here, in a 5-year garden experiment on two short-lived, otherwise non-clonal species, Barbarea vulgaris and Barbarea stricta, we compared the fitness of plants fragmented by simulated disturbance ("enforced ramets") both with plants that contemporaneously originate in seed and with individuals unscathed by the disturbance event. Because the ability to regrow from fragments is related to plant age and stored reserves, we compared the effects of disturbance applied during three different ontogenetic stages of the plants. In B. vulgaris, enforced ramet fitness was higher than the measured fitness values of both uninjured plants and plants established from seed after the disturbance. This advantage decreased with increasing plant age at the time of fragmentation. In B. stricta, enforced ramet fitness was lower than or similar to fitness of uninjured plants and plants grown from seed. Our results likely reflect the habitat preferences of the study species, as B. vulgaris occurs in anthropogenic, disturbed habitats where body fragmentation is more probable and enforced clonality thus more advantageous than in the more natural habitats preferred by B. stricta. Generalizing from our results, we see that increased fitness yielded by enforced clonality would confer an evolutionary advantage in the face of disturbance, especially in habitats where a seed bank has not been formed, e.g., during invasion or colonization. Our results thus imply that enforced clonality should be taken into account when studying population dynamics and life strategies of otherwise non-clonal species in disturbed habitats.

Department of Functional Ecology Institute of Botany Czech Academy of Sciences Třeboň Czech Republic

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Anderson M. J., Gorley R. N., Clarke K. R. (2008). PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth: PRIMER-E.

Bailey J. P., Bímová K., Mandák B. (2009). Asexual spread versus sexual reproduction and evolution in Japanese Knotweed s.l. sets the stage for the “Battle of the Clones”. Biol. Invasions 11, 1189–1203. 10.1007/s10530-008-9381-4 DOI

Barrat-Segretain M. H., Bornette G. (2000). Regeneration and colonization abilities of aquatic plant fragments: effect of disturbance seasonality. Hydrobiologia 421, 31–39. 10.1023/A:1003980927853 DOI

Bartušková A., Klimešová J. (2010). Reiteration in the short lived root-sprouting herb Rorippa palustris: does the origin of buds matter? Botany 88, 630–638. 10.1139/B10-044 DOI

Baskin C. C., Baskin J. M. (1998). Seeds. Ecology, Biogeography, and Evolution of Dormancy and Germination. San Diego, CA: Academic Press.

Baskin J. M., Baskin C. C. (1989). Seasonal changes in the germination responses of buried seeds of Barbarea vulgaris. Can. J. Bot. 67, 2131–2134. 10.1139/b89-269 DOI

Bazot S., Barthes L., Blanot D., Fresneau C. (2013). Distribution of non-structural nitrogen and carbohydrate compounds in mature oak trees in a temperate forest at four key phenological stages. Trees Struct. Funct. 27, 1023–1034. 10.1007/s00468-013-0853-5 DOI

Bewley J. D. (1997). Seed germination and dormancy. Plant Cell 9, 1055–1066. 10.1105/tpc.9.7.1055 PubMed DOI PMC

Bímová K., Mandák B., Pyšek P. (2003). Experimental study of vegetative regeneration in four invasive Reynoutria taxa (Polygonaceae). Plant Ecol. 166, 1–11. 10.1023/A:1023299101998 DOI

Birlanga V., Villanova J., Cano A., Cano E. A., Acosta M., Perez-Perez J. M. (2015). Quantitative analysis of adventitious root growth phenotypes in carnation stem cuttings. PLoS ONE 10:e0133123. 10.1371/journal.pone.0133123 PubMed DOI PMC

Boedeltje G., Bakker J. P., Bekker R. M., Van Groenendael J. M., Soesbergen M. (2003). Plant dispersal in a lowland stream in relation to occurrence and three specific life-history traits of the species in the species pool. J. Ecol. 91, 855–866. 10.1046/j.1365-2745.2003.00820.x DOI

Campbell M. L. (2003). Recruitment and colonisation of vegetative fragments of Posidonia australis and Posidonia coriacea. Aquat. Bot. 76, 175–184. 10.1016/S0304-3770(03)00016-0 DOI

Collins W. J. (1981). The effects of length of growing season, with and without defoliation, on seed yield and hard-seededness in swards of subterranean clover. Aust. J. Agric. Res. 32, 783–792. 10.1071/AR9810783 DOI

de Souza J. C. A. V., Bender A. G., Tivano J. C., Barroso D. G., Mroginski L. A., Vegetti A. C., et al. (2014). Rooting of Prosopis alba mini-cuttings. New Forest. 45, 745–752. 10.1007/s11056-014-9429-5 DOI

Dietz H., Köhler A., Ullmann I. (2002). Regeneration growth of the invasive clonal forb Rorippa austriaca (Brassicaceae) in relation to fertilization and interspecific competition. Plant Ecol. 158, 171–182. 10.1023/A:1015567316004 DOI

Dvořák F. (1992). 14. Barbarea R. Br, in Flora of the Czech Republic, Vol. 3, eds Hejnı S., Slavík S. (Praha: Academia; ), 72–76.

Elgersma K. J., Wildová R., Martina J. P., Currie W. S., Goldberg D. E. (2015). Does clonal resource translocation relate to invasiveness of Typha taxa? Results from a common garden experiment. Aquat. Bot. 126, 48–53. 10.1016/j.aquabot.2015.06.008 DOI

Fenner M. (1995). Ecology of seed banks, in Seed Development and Germination, eds Kigel J., Galili G. (New York, NY: Ademic Press; ), 507–528.

Fukui S., Araki K. S. (2014). Spatial niche facilitates clonal reproduction in seed plants under temporal disturbance. PLoS ONE 9:e116111. 10.1371/journal.pone.0116111 PubMed DOI PMC

Galen C., Stanton M. L. (1991). Consequences of emergence phenology for reproductive success in Ranunculus adoneus (Ranunculaceae). Am. J. Bot. 78, 978–988. 10.2307/2445177 DOI

Gioria M., Pyšek P., Moravcová L. (2012). Soil seed banks in plant invasions: promoting species invasiveness and long-term impact on plant community dynamics. Preslia 84, 327–350.

Glover R., Drenovsky R. E., Futrell C. J., Grewell B. J. (2015). Clonal integration in Ludwigia hexapetala under different light regimes. Aquat. Bot. 122, 40–46. 10.1016/j.aquabot.2015.01.004 DOI

Groff P. A., Kaplan D. R. (1988). The relation of root systems in vascular plants. Bot. Rev. 54, 387–422. 10.1007/BF02858417 DOI

Hess E. (1909). Uber die Wuchsformen der Alpinen Gerollpflanzen. Arbeit aus dem Botanischen Museum des Eidg. Dresden: Polytechnikum Zurich, Druck von C. Heinrich.

Hintikka V. (1988). Induction of secondary dormancy in seeds of Barbarea stricta and B. vulgaris by chlormequat and daminozide, and its termination by gibberellic acid. Weed Res. 28, 7–11. 10.1111/j.1365-3180.1988.tb00779.x DOI

Huhta A. P., Rautio P., Hellstrom K., Saari M., Tuomi J. (2009). Tolerance of a perennial herb, Pimpinella saxifraga, to simulated flower herbivory and grazing: immediate repair of injury or postponed reproduction? Plant Ecol. 201, 599–609. 10.1007/s11258-008-9535-6 PubMed DOI

Kaur J., Percival D., Hainstock L. J., Prive J. P. (2012). Seasonal growth dynamics and carbon allocation of the wild blueberry plant (Vaccinium angustifolium Ait.). Can. J. Plant. Sci. 92, 1145–1154. 10.4141/cjps2011-204 DOI

Kefford N. P., Caso O. H. (1972). Organ regeneration on excised roots of Chondilla juncea and its chemical regulation. Aust. J. Biol. Sci. 25, 691–706.

Klimeš L., Klimešová J., Hendriks R., van Groenendael J. (1997). Clonal plant architecture: a comparative analysis of form and function, in The Ecology and Evolution of Clonal Plants, eds de Kroon H., van Groenendael J. (Leiden: Backhuys Publishers; ), 3–29.

Klimešová J., Klimeš L. (2007). Bud banks and their role in vegetative regeneration - A literature review and proposal for simple classification and assessment. Perspect. Plant Ecol. 8, 115–129. 10.1016/j.ppees.2006.10.002 DOI

Klimešová J., Kociánová A., Martínková J. (2008). Weeds that can do both tricks: vegetative versus generative regeneration of the short-lived root-sprouting herbs Rorippa palustris and Barbarea vulgaris. Weed Res. 48, 131–135. 10.1111/j.1365-3180.2007.00608.x DOI

Klimešová J., Martínková J. (2004). Intermediate growth forms as a model for the study of plant clonality functioning: an example with root sprouters. Evol. Ecol. 18, 669–681. 10.1007/s10682-004-5149-1 DOI

Klimešová J., Sosnová M., Martínková J. (2007). Life-history variation in the short-lived herb Rorippa palustris: effect of germination date and injury timing. Plant Ecol. 189, 237–246. 10.1007/s11258-006-9180-x DOI

Leakey R. R. B., Chancellor R. J., Vince-Prue D. (1977). Regeneration from rhizome fragments of Agropyron repens. I. The seasonality of shoot growth and rhizome reserves in single node fragments. Ann. App. Biol. 87, 423–432. 10.1111/j.1744-7348.1977.tb01907.x DOI

Li X. X., Shen Y. D., Huang Q. Q., Fan Z. W., Huang D. D. (2013). Regeneration capacity of small clonal fragments of the invasive Mikania micrantha H.B.K.: effects of burial depth and stolon internode length. PLoS ONE 8:e84657. 10.1371/journal.pone.0084657 PubMed DOI PMC

Lin H. F., Alpert P., Yu F. H. (2012). Effects of fragment size and water depth on performance of stem fragments of the invasive, amphibious, clonal plant Ipomoea aquatica. Aquat. Bot. 99, 34–40. 10.1016/j.aquabot.2012.01.004 DOI

MacDonald M. A., Cavers P. B. (1991). The biology of Canadian weeds. 97. Barbarea vulgaris R. Br. Can. J. Plant Sci. 71, 149–166. 10.4141/cjps91-016 DOI

Martínková J., Klimešová J., Mihulka S. (2008). Compensation of seed production after severe injury in the short-lived herb Barbarea vulgaris. Basic Appl. Ecol. 1, 44–54. 10.1016/j.baae.2006.12.001 DOI

Martínková J., Šmilauer P., Mihulka S., Latzel V., Klimešová J. (2016). The effect of injury on whole-plant senescence: an experiment with two root-sprouting Barbarea species. Ann. Bot. Available online at: http://www.oxfordjournals.org/our_journals/annbot/recently_accepted_papers.html PubMed PMC

McIntyre G. I. (1972). Developmental studies on Euphorbia esula – Influence of nitrogen supply on correlative inhibition of root bud activity. Can. J. Bot. 50, 949–956. 10.1139/b72-115 DOI

Meloni M., Reid A., Caujapé-Castells J., Marrero A., Fernández-Palacios J. M., Mesa-Coelo R. A., et al. . (2013). Effects of clonality on the genetic variability of rare, insular species: the case of Ruta microcarpa from the Canary Islands. Ecol. Evol. 3, 1569–1579. 10.1002/ece3.571 PubMed DOI PMC

Monty A., Eugène M., Mahy G. (2015). Vegetative regeneration capacities of five ornamental plant invaders after shredding. Environ. Manage. 55, 423–430. 10.1007/s00267-014-0398-4 PubMed DOI

Noble I. R., Slatyer R. O. (1980). The use of vital attributes to predict successional changes in plant communities subjected to recurrent disturbance. Vegetatio 43, 5–21. 10.1007/BF00121013 DOI

Piippo S., Hellstrom K., Huhta A. P., Rautio P., Tuomi J. (2009). Delayed flowering as a potential benefit-decreasing cost of compensatory regrowth. Botany 87, 837–844. 10.1139/B09-057 DOI

Roberts-Nkrumah L. B. (2006). Cultivar and cultural factors affecting adventitious shoot production on breadfruit root cuttings. Trop. Agric. 83, 54–60.

Sagers C. L. (1993). Reproduction in neotropical shrubs – The occurrence and some mechanisms of asexuality. Ecology 74, 615–618. 10.2307/1939321 DOI

Sampliner D., Miller A. (2009). Ethnobotany of horseradish (Armoracia rusticana, Brassicaceae) and its wild relatives (Armoracia spp.): reproductive biology and local uses in their native ranges. Econ. Bot. 63, 303–313. 10.1007/s12231-009-9088-1 DOI

Shepherd M., Rose T., Raymond C. (2013). Rejuvenation of mature native tea tree (Melaleuca alternifolia (maiden & betche) cheel) for vegetative propagation. Propag. Ornam. Plants 13, 103–111.

Simpson A. G., Gendall A. R., Dean C. (1999). When to switch to flowering. Annu. Rev. Cell. Dev. Biol. 15, 519–550. 10.1146/annurev.cellbio.15.1.519 PubMed DOI

Sosnová M., Herben T., Martínková J., Bartušková A., Klimešová J. (2014). To resprout or not to resprout? Modeling population dynamics of a root-sprouting monocarpic plant under various disturbance regimes. Plant Ecol. 216, 901–911. 10.1007/s11258-014-0382-3 DOI

Sosnová M., Klimešová J. (2009). Life-history variation in the short-lived herb Rorippa palustris: the role of carbon storage. Acta Oecol. 35, 691–697. 10.1016/j.actao.2009.06.010 DOI

Thomsen M. G., Brandsaeter L. O., Fykse H. (2013). Regeneration of Canada thistle (Cirsium arvense) from intact roots and root fragments at different soil depths. Weed Sci. 61, 277–282. 10.1614/WS-D-12-00095.1 DOI

Tolsma A. D., Tolhurst K. G., Read S. M. (2010). Effects of fire, post-fire defoliation, drought and season on regrowth and carbohydrate reserves of alpine snowgrass Poa fawcettiae (Poaceae). Aust. J. Bot. 58, 57–168. 10.1071/BT09186 DOI

Wang Z. W., van Kleunen M., During H. J., Werger M. J. A. (2013). Root foraging increases performance of the clonal plant Potentilla reptans in heterogeneous nutrient environments. PLoS ONE 8:e58602. 10.1371/journal.pone.0058602 PubMed DOI PMC

Wehsarg O. (1954). Ackerunkrauter. Berlin: Akademie Verlag.

Wilson S. D., Tilman D. (1993). Plant competition and resource availability in response to disturbance and fertilization. Ecology 74, 599–611. 10.2307/1939319 DOI

Comparative analysis of root sprouting and its vigour in temperate herbs: anatomical correlates and environmental predictors