Abstract
Under climate change, regeneration from seeds is becoming increasingly important for species persistence, migration and conservation, especially in high-elevation environments. In this regard, the ability of seeds to remain viable for a long time is a crucial prerequisite for seed persistence in the soil and in germplasm banks. However, little is known about the effects of climate warming on seed longevity of alpine plants. Here, we analysed the effects of a moderately warmer parental growth environment generated by open top chambers on subsequent seed longevity of four alpine snowbed species. Seeds from plants exposed to natural and warmed climate during the growing season were subjected to laboratory-controlled accelerated ageing and then regularly sampled for germination tests. Initial viability (Ki), deterioration rate (σ −1) and time taken for viability to fall to 50 % (p 50) were estimated using probit analysis. Across species and treatments, p 50 varied from 4.9 to 23.1 days. Seeds produced by plants exposed to warmer temperatures were significantly longer lived than those from plants at natural conditions. Under warming, the seed progeny showed either a higher Ki or a slower σ −1. Under moderate climate warming (about + 2 K), alpine snowbed species produced seeds with an extended resistance to heat stress indicating an effective rapid response to the new environment. Such plastic response may play a key role for survival and persistence of alpine snowbed species facing climate change and may also have important implications for ex situ conservation.
Similar content being viewed by others
References
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki N (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New York
Björk RG, Molau U (2007) Ecology of alpine snowbeds and the impact of global change. Arct Antarct Alp Res 39:34–43
Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–190
Boyko A, Blevins T, Yao Y et al (2010) Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS One 5:e9514. doi:10.1371/journal.pone.0009514
Carbognani M, Petraglia A, Tomaselli M (2012) Influence of snowmelt time on species richness, density and production in a late snowbed community. Acta Oecol 43:113–120
Carbognani M, Tomaselli M, Petraglia A (2014a) Current vegetation changes in an alpine late snowbed community in the southeastern Alps (N-Italy). Alp Bot 124:105–113
Carbognani M, Petraglia A, Tomaselli M (2014b) Warming effects and plant trait control on the early-decomposition in alpine snowbeds. Plant Soil 376:277–290
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366
Diekmann M, Frison EA, Putter T (1994) FAO/IPGRI technical guidelines for the safe movement of small fruit germoplasm. Food and Agriculture Organisation of the United Nations/International Plant Genetic Resource Institute, Rome
Donohue K (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philos Trans R Soc B 364:1059–1074
Ellis RH, Hong TD (1994) Desiccation tolerance and potential longevity of developing seeds of rice (Oryza sativa L.). Ann Bot 73:501–550
Ellis RH, Roberts EH (1980) Improved equations for the prediction of seed longevity. Ann Bot 45:13–30
Ellis RH, Hong TD, Jackson MT (1993) Seed production environment, time of harvest, and the potential longevity of seeds of three cultivars of rice (Oryza sativa L.). Ann Bot 72:583–590
Elumeeva TG, Onipchenko VG, Egorov AV et al (2013) Long-term vegetation dynamic in the Northwestern Caucasus: which communities are more affected by upward shifts of plant species? Alp Bot 123:77–85
Facelli JM, Chesson P, Barnes N (2005) Differences in seed biology of annual plants in arid lands: a key ingredient of the storage effect. Ecology 86:2998–3006
Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136
Gottfried M, Pauli H, Futschik A et al (2012) Continent-wide response of mountain vegetation to climate change. Nat Clim Change 2:111–115
Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain plants. Nature 369:448
Hay F (2004) The seed viability equations. http://data.kew.org/sid/viability/SeedViabilityEquationsFHDec04.pdf. Accessed 19 Aug 2013
Hay FR, Probert RJ (1995) Seed maturity and the effects of different drying conditions on desiccation tolerance and seed longevity in foxglove (Digitalis purpurea L.). Ann Bot 76:639–647
Hay FR, Smith RD (2003) Seed maturity: when to collect seeds from wild plants. In: Smith RD, Dickie JB, Linnington SH, Pritchard HW, Probert RJ (eds) Seed conservation: turning science into practice. Royal Botanic Gardens, Kew, London, pp 97–133
Hay FR, Adams J, Manger K, Probert RJ (2008) The use of non-saturated lithium chloride solutions for experimental control of seed water content. Seed Sci Technol 36:737–746
Herman JJ, Sultan SE (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front Plant Sci 2:102. doi:10.3389/fpls.2011.00102
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Hoyle GL, Steadman KJ, Daws MI, Adkins SW (2008) Pre- and post-harvest influences on seed dormancy status of an Australian Goodeniaceae species, Goodenia fascicularis. Ann Bot 102:93–101
Hoyle GL, Venn SE, Steadman KJ et al (2013) Soil warming increases plant species richness but decreases germination from the alpine soil seed bank. Glob Change Biol 19:1549–1561
International Panel on Climate Change (IPCC) et al (2013) Summary for policymackers. In: Stocker TF, Qin D, Plattner G-K (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 3–29
Klanderud K, Totland Ø (2005) Simulated climate change altered dominance hierarchies and diversity of an alpine biodiversity hotspot. Ecology 86:2047–2054
Kochanek J (2008) Parental Growth Environment Modulates Seed Longevity: Investigations Using Australian Native Species. PhD Thesis, University of Queensland, Australia
Kochanek J, Steadman KJ, Probert RJ, Adkins SW (2011) Parental effects modulate seed longevity: exploring parental and offspring phenotypes to elucidate pre-zygotic environmental influences. New Phytol 191:223–233
Körner C, Cochrane P (1983) Influence of plant physiognomy on leaf temperature on clear midsummer days in the Snowy Mountains, south-eastern Australia. Acta Oecol Oecol Plant 4:117–124
Kou HP, Li Y, Song XX et al (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 168:1685–1693
Larcher W, Wagner J (1976) Temperaturgrenzen der CO2-Aufnahme und Temperaturresistenz der Blätter von Gebirgspflanzen im vegetationsaktiven Zustand. Oecol Plant 11:361–374
Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771
Long RL, Panetta FD, Steadman KJ et al (2008) Seed persistence in the field may be predicted by laboratory-controlled aging. Weed Sci 56:523–528
Luzuriaga AL, Escudero A, Pérez-García F (2006) Environmental maternal effects on seed morphology and germination in Sinapis arvensis (Cruciferae). Weed Res 46:163–174
Marion GM, Henry GHR, Freckman DW et al (1997) Open-top design for manipulating field temperature in high-latitude ecosystems. Glob Change Biol 3:20–32
Meyer SE, Allen PS (1999) Ecological genetics of seed germination regulation in Bromus tectorum L. II. Reaction norms in response to a water stress gradient imposed during seed maturation. Oecologia 20:35–43
Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296
Mondoni A, Probert RJ, Rossi G, Vegini E, Hay FR (2011) Seeds of alpine plants are short lived: implications for long-term conservation. Ann Bot 107:171–179
Mondoni A, Rossi G, Orsenigo S, Probert RJ (2012) Climate warming could shift the timing of seed germination in alpine plants. Ann Bot 110:155–164
Mondoni A, Orsenigo S, Donà M et al (2014) Environmental-induced transgenerational changes in seed longevity: maternal and genetic influence. Ann Bot 113:1257–1263
Mondoni A, Pedrini S, Bernareggi G et al (2015) Climate warming could increase recruitment success in glacier foreland plants. Ann Bot. doi:10.1093/aob/mcv101
Murdoch AJ, Ellis RH (2000) Dormancy, viability and longevity. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI Publishing, New York, pp 183–214
Newton R, Hay F, Probert R (2009) Protocol for comparative seed longevity testing. Technical Information Sheet_01, Royal Botanic Gardens Kew, UK. http://www.kew.org/sites/default/files/1_ppcont_014163_Protocol%20for%20comparative%20seed%20longevity%20testing_0.pdf. Accessed 8 Nov 2013
Nicotra AB, Atkin OK, Bonser SP et al (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–690
Ooi MJ, Auld T, Denham AJ (2009) Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Glob Change Biol 15:2375–2386
Parolo G, Rossi G (2008) Upward migration of vascular plants following a climate warming trend in the Alps. Basic Appl Ecol 9:100–107
Petraglia A, Tomaselli M, Petit Bon M et al (2014) Responses of flowering phenology of snowbed plants to an experimentally imposed extreme advanced snowmelt. Plant Ecol 215:759–768
Probert RJ, Daws MI, Hay FR (2009) Ecological correlates of ex situ seed longevity: a comparative study on 195 species. Ann Bot 104:57–69
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Roberts EH (1973) Predicting the storage life of seeds. Seed Sci Technol 1:499–514
Sandvik SM, Odland A (2013) Changes in alpine snowbed-wetland vegetation over three decades in northern Norway. Nord J Bot 32:377–384
Sandvik SM, Heegaard E, Elven R, Vandvik V (2004) Responses of alpine snowbed vegetation to long-term experimental warming. Ecoscience 11:150–159
Sanhewe AJ, Ellis RH (1996) Seed development and maturation in Phaseolus vulgaris. I. Ability to germinate and to tolerate desiccation. J Exp Bot 47:949–958
Schöb C, Kammer PM, Kikvidze Z, Choler P, Veit H (2008) Changes in species composition in alpine snowbeds with climate change inferred from small-scale spatial patterns. Web Ecol 8:142–159
Schwienbacher E, Erschbamer B (2001) Longevity of seeds in a glacier foreland of the Central Alps—a burial experiment. Bulletin of the Geobotanical Institute ETH 68:63–71
Schwienbacher E, Marcante S, Erschbamer B (2010) Alpine species seed longevity in the soil in relation to seed size and shape—a 5-year burial experiment in the Central Alps. Flora 205:19–25
Shevtsova A, Graae BJ, Jochum T et al (2009) Critical periods for impact of climate warming on early seedling establishment in subarctic tundra. Glob Change Biol 15:2662–2680
Sinniah UR, Ellis RH, John P (1998) Irrigation and seed quality development in rapid-cycling Brassica: seed germination and longevity. Ann Bot 82:309–314
Theurillat JP, Guisan A (2001) Potential impact of climate change on vegetation in the European Alps: a review. Clim Change 50:77–109
Violle CJ, Enquist BJ, McGill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252
Virtanen R, Eskelinen A, Gaare E (2003) Long-term changes in alpine plant communities in Norway and Finland. In: Nagy L, Grabherr G, Körner C, Thompson DBA (eds) Alpine biodiversity in Europe. Springer-Verlag, Berlin, pp 411–422
Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011) Climate change and plant regeneration from seed. Glob Change Biol 17:2145–2161
Walters C, Wheeler LM, Grotenhuis JM (2005) Longevity of seeds stored in a genebank: species characteristics. Seed Sci Res 15:1–20
Whittle CA, Otto SP, Johnston MO, Krochko JE (2009) Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany 87:650–657
Acknowledgments
We thank the Stelvio National Park for fieldwork authorization and the two anonymous reviewers for their useful comments on this manuscript. We also thank Janet Prevey for the English revision.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bernareggi, G., Carbognani, M., Petraglia, A. et al. Climate warming could increase seed longevity of alpine snowbed plants. Alp Botany 125, 69–78 (2015). https://doi.org/10.1007/s00035-015-0156-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-015-0156-0