Aciphylla glacialis mortality, growth and frost resistance: a field warming experiment
Sonya R. Geange
A B , Meisha-Marika Holloway-Phillips A , Veronica F. Briceño A and Adrienne B. Nicotra A
+ Author Affiliations
- Author Affiliations
A Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.
B Corresponding author. Email: sonya.geange@anu.edu.au
Australian Journal of Botany 67(8) 599-609 https://doi.org/10.1071/BT19034
Submitted: 27 February 2019 Accepted: 30 October 2019 Published: 10 February 2020
Abstract
Decreasing snow depth and earlier snowmelt in alpine regions are expected to expose plants to a greater range of thermal extremes. Thus, paradoxically, in addition to increasing mean temperatures, aseasonal frost is likely to emerge as a major determinant of plant survival and development under a warming climate. Through the use of open top chambers, we assessed the effects of simulated warming on seedlings of the alpine herb Aciphylla glacialis (F.Muell.) Benth, sourced from provenances that vary in thermal characteristics. We hypothesised that seedlings grown at elevated temperature would have reduced survival and lower freezing resistance, but that individuals that did survive would show increased growth. Further, we hypothesised that seedlings sourced from the lower-elevation sites, where temperatures are more variable, would exhibit lower mortality at warmed conditions than those from sites with narrower thermal ranges. Warmed conditions significantly increased seedling mortality but those that survived grew slightly taller than their ambient counterparts, with no impact on leaf production or photosynthetic efficiency. Although the warming treatment did not influence temperature minimums, which would have allowed us to assess the impact of aseasonal frosts, there was no effect on freezing resistance. Contrary to our expectations, there was little evidence of variation among provenances. Our results indicate that a warmer climate with more extreme events may lead to a reduction in seedling establishment and survival; however, seedlings that do survive and establish are unlikely to express any lingering detrimental effects.
Additional keywords: ice nucleation, intraspecific variation, open top chambers, phenotypic plasticity, transplant experiment.
References
Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings. of the Royal Society B. Biological Sciences 279, 3843–3852.| Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change.Crossref | GoogleScholarGoogle Scholar |
Aragon-Gastelum JL, Badano E, Yanez-Espinosa L, Ramirez-Tobias HM, Rodas-Ortiz JP, Gonzalez-Salvatierra C, Flores J (2017) Seedling survival of three endemic and threatened Mexican cacti under induced climate change. Plant Species Biology 32, 92–99.
| Seedling survival of three endemic and threatened Mexican cacti under induced climate change.Crossref | GoogleScholarGoogle Scholar |
Armbruster S, Rae DA, Edwards ME (2007) Topographic complexity and terrestrial biotic response to high-latitude climate change: Variance is as important as the mean. In ‘Arctic alpine ecosystems and people in a changing environment’. (Eds JB Ørbæk, R Kallenborn, I Tombre, EN Hegseth, S Falk-Petersen, AH Hoel) pp. 105–121. (Springer: Berlin)
Auge GA, Leverett LD, Edwards BR, Donohue K (2017) Adjusting phenotypes via within- and across-generational plasticity. New Phytologist 216, 343–349.
| Adjusting phenotypes via within- and across-generational plasticity.Crossref | GoogleScholarGoogle Scholar | 28262950PubMed |
Ball MC, Harris-Pascal D, Egerton JJG, Lenne T (2012) The paradoxical increase in freezing injury in a warming climate: frost as a driver of change in cold climate vegetation. Temperature Adaptation in a Changing Climate: Nature at Risk 3, 179–185.
Bannister P (2007) Godley review: a touch of frost? Cold hardiness of plants in the southern hemisphere. New Zealand Journal of Botany 45, 1–33.
| Godley review: a touch of frost? Cold hardiness of plants in the southern hemisphere.Crossref | GoogleScholarGoogle Scholar |
Bannister P, Maegli T, Dickinson KJ, Halloy SR, Knight A, Lord JM, Mark AF, Spencer KL (2005) Will loss of snow cover during climatic warming expose New Zealand alpine plants to increased frost damage? Oecologia 144, 245–256.
| Will loss of snow cover during climatic warming expose New Zealand alpine plants to increased frost damage?Crossref | GoogleScholarGoogle Scholar | 15891822PubMed |
Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Beniston M (2003) Climatic change in mountain regions: a review of possible impacts. Climatic Change 59, 5–31.
| Climatic change in mountain regions: a review of possible impacts.Crossref | GoogleScholarGoogle Scholar |
Billings WD, Bliss LC (1959) An Alpine snowbank environment and its effects on vegetation, plant development, and productivity. Ecology 40, 388–397.
| An Alpine snowbank environment and its effects on vegetation, plant development, and productivity.Crossref | GoogleScholarGoogle Scholar |
Bischoff A, Müller-Schärer H (2010) Testing population differentiation in plant species - how important are environmental maternal effects. Oikos 119, 445–454.
| Testing population differentiation in plant species - how important are environmental maternal effects.Crossref | GoogleScholarGoogle Scholar |
Bradshaw AD (2006) Unravelling phenotypic plasticity – why should we bother? New Phytologist 170, 644–648.
| Unravelling phenotypic plasticity – why should we bother?Crossref | GoogleScholarGoogle Scholar | 16684227PubMed |
Bradshaw AD, Hardwick K (1989) Evolution and stress – genotypic and phenotypic components. Biological Journal of the Linnean Society. Linnean Society of London 37, 137–155.
| Evolution and stress – genotypic and phenotypic components.Crossref | GoogleScholarGoogle Scholar |
Bradshaw WE, Holzapfel CM (2006) Climate change. Evolutionary response to rapid climate change. Science 312, 1477–1478.
| Climate change. Evolutionary response to rapid climate change.Crossref | GoogleScholarGoogle Scholar | 16763134PubMed |
Briceno VF (2014) Thermal microenvironments and the ecology of the alpine herb Aciphylla glacialis. PhD thesis, The Australian National University, Research School of Biology, ACT, Australia.
Briceno VF, Harris-Pascal D, Nicotra AB, Williams E, Ball MC (2014) Variation in snow cover drives differences in frost resistance in seedlings of the alpine herb Aciphylla glacialis. Environmental and Experimental Botany 106, 174–181.
| Variation in snow cover drives differences in frost resistance in seedlings of the alpine herb Aciphylla glacialis.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2019) Climate statistics for Australian locations: Monthly climate statistics. Summary statistics THREDBO AWS (Station 071032). Available at: http://www.bom.gov.au/climate/averages/tables/cw_071032.shtml
Camac JS, Williams RJ, Wahren C-H, Hoffmann AA, Vesk PA (2017) Climatic warming strengthens a positive feedback between alpine shrubs and fire. Global Change Biology 23, 3249–3258.
| Climatic warming strengthens a positive feedback between alpine shrubs and fire.Crossref | GoogleScholarGoogle Scholar | 28063181PubMed |
Cochrane JA, Hoyle GL, Yates CJ, Wood J, Nicotra AB (2015) Climate warming delays and decreases seedling emergence in a Mediterranean ecosystem. Oikos 124, 150–160.
| Climate warming delays and decreases seedling emergence in a Mediterranean ecosystem.Crossref | GoogleScholarGoogle Scholar |
Costin AB, Gray M, Totterdell C, Wimbush D (2000) ‘Kosciuszko alpine flora.’ (CSIRO Publishing: Melbourne)
Davis CJ (2013) Towards the development of long-term winter records for the Snowy Mountains. Australian Meteorological and Oceanographic Journal 63, 303–313.
| Towards the development of long-term winter records for the Snowy Mountains.Crossref | GoogleScholarGoogle Scholar |
Galen C, Stanton ML (1993) Short-term responses of alpine buttercups to experimental manipulations of growing-season length. Ecology 74, 1052–1058.
| Short-term responses of alpine buttercups to experimental manipulations of growing-season length.Crossref | GoogleScholarGoogle Scholar |
Galen C, Stanton ML (1995) Responses of snowbed plant-species to changes in growing-season length. Ecology 76, 1546–1557.
| Responses of snowbed plant-species to changes in growing-season length.Crossref | GoogleScholarGoogle Scholar |
Gerdol R, Siffi C, Iacumin P, Gualmini M, Tomaselli M (2013) Advanced snowmelt affects vegetative growth and sexual reproduction of Vaccinium myrtillus in a sub-alpine heath. Journal of Vegetation Science 24, 569–579.
| Advanced snowmelt affects vegetative growth and sexual reproduction of Vaccinium myrtillus in a sub-alpine heath.Crossref | GoogleScholarGoogle Scholar |
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394–407.
| Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments.Crossref | GoogleScholarGoogle Scholar |
Green K, Pickering CM (2009) The decline of snowpatches in the Snowy Mountains of Australia: importance of climate warming, variable snow, and wind. Arctic, Antarctic, and Alpine Research 41, 212–218.
| The decline of snowpatches in the Snowy Mountains of Australia: importance of climate warming, variable snow, and wind.Crossref | GoogleScholarGoogle Scholar |
Hacker J, Neuner G (2008) Ice propagation in dehardened alpine plant species studied by Infrared Differential Thermal Analysis (IDTA). Arctic, Antarctic, and Alpine Research 40, 660–670.
| Ice propagation in dehardened alpine plant species studied by Infrared Differential Thermal Analysis (IDTA).Crossref | GoogleScholarGoogle Scholar |
Harris RMB, Remenyi TA, Bindoff NL (2016) The potential impacts of climate change on Victorian alpine resorts. A report to the Alpine Resorts Co-ordinating Council. Antartic Climate and Ecosystems Cooperative Research Centre, Hobart, Australia.
Harris RMB, Beaumont LJ, Vance TR, Tozer CR, Remenyi TA, Perkins-Kirkpatrick SE, Mitchell PJ, Nicotra AB, McGregor S, Andrew NR, Letnic M, Kearney MR, Wernberg T, Hutley LB, Chambers LE, Fletcher M-S, Keatley MR, Woodward CA, Williamson G, Duke NC, Bowman DMJS (2018) Biological responses to the press and pulse of climate trends and extreme events. Nature Climate Change 8, 579–587.
| Biological responses to the press and pulse of climate trends and extreme events.Crossref | GoogleScholarGoogle Scholar |
Hennessy KJ, Whetton PH, Walsh K, Smith IN, Bathols JM, Hutchinson M, Sharples J (2008) Climate change effects on snow conditions in mainland Australia and adaptation at ski resorts through snowmaking. Climate Research 35, 255–270.
| Climate change effects on snow conditions in mainland Australia and adaptation at ski resorts through snowmaking.Crossref | GoogleScholarGoogle Scholar |
Hoyle GL, Cordiner H, Good RB, Nicotra AB (2014) Effects of reduced winter duration on seed dormancy and germination in six populations of the alpine herb Aciphyllya glacialis (Apiaceae). Conservation Physiology 2, cou015
| Effects of reduced winter duration on seed dormancy and germination in six populations of the alpine herb Aciphyllya glacialis (Apiaceae).Crossref | GoogleScholarGoogle Scholar | 27293636PubMed |
Hughes L (2003) Climate change and Australia: trends, projections and impacts. Austral Ecology 28, 423–443.
| Climate change and Australia: trends, projections and impacts.Crossref | GoogleScholarGoogle Scholar |
Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecology Letters 3, 457–463.
| The ecological and evolutionary significance of frost in the context of climate change.Crossref | GoogleScholarGoogle Scholar |
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89, 353–362.
| Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers.Crossref | GoogleScholarGoogle Scholar | 18409425PubMed |
IPCC (2014 )
Jordan DN, Smith WK (1994) Energy balance analysis of nighttime leaf temperatures and frost formation in a subalpine environment. Agricultural and Forest Meteorology 71, 359–372.
| Energy balance analysis of nighttime leaf temperatures and frost formation in a subalpine environment.Crossref | GoogleScholarGoogle Scholar |
Körner C (2003) ‘Alpine plant life.’ 2nd edn. (Springer: New York)
Körner C, Hiltbrunner E (2018) The 90 ways to describe plant temperature. Perspectives in Plant Ecology, Evolution and Systematics 30, 16–21.
| The 90 ways to describe plant temperature.Crossref | GoogleScholarGoogle Scholar |
Kudernatsch T, Fischer A, Bernhardt-Romermann M, Abs C (2008) Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic and Applied Ecology 9, 263–274.
| Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species.Crossref | GoogleScholarGoogle Scholar |
Kudo G, Suzuki S (2003) Warming effects on growth, production, and vegetation structure of alpine shrubs: a five-year experiment in northern Japan. Oecologia 135, 280–287.
| Warming effects on growth, production, and vegetation structure of alpine shrubs: a five-year experiment in northern Japan.Crossref | GoogleScholarGoogle Scholar | 12698350PubMed |
Larcher W, Kainmuller C, Wagner J (2010) Survival types of high mountain plants under extreme temperatures. Flora 205, 3–18.
| Survival types of high mountain plants under extreme temperatures.Crossref | GoogleScholarGoogle Scholar |
Lenoir J, Hattab T, Pierre G (2017) Climatic microrefugia under anthropogenic climate change: implications for species redistribution. Ecography 40, 253–266.
| Climatic microrefugia under anthropogenic climate change: implications for species redistribution.Crossref | GoogleScholarGoogle Scholar |
Lindenmayer DB, Likens GE, Andersen A, Bowman D, Michael Bull C, Burns E, Dickman CR, Hoffmann AA, Keith DA, Liddell MJ, et al (2012) Value of long-term ecological studies. Austral Ecology 37, 745–757.
| Value of long-term ecological studies.Crossref | GoogleScholarGoogle Scholar |
Luca AD, Evans JP, Ji F (2018) Australian snowpack in the NARCliM ensemble: evaluation, bias correction and future projections. Climate Dynamics 51, 639–666.
| Australian snowpack in the NARCliM ensemble: evaluation, bias correction and future projections.Crossref | GoogleScholarGoogle Scholar |
Marquez EJ, Rada F, Farinas MR (2006) Freezing tolerance in grasses along an altitudinal gradient in the Venezuelan Andes. Oecologia 150, 393–397.
| Freezing tolerance in grasses along an altitudinal gradient in the Venezuelan Andes.Crossref | GoogleScholarGoogle Scholar | 17024382PubMed |
Mazerolle MJ (2016) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package ver. 2.1-0 edn. Available at: https://cran.r-project.org/package=AICcmodavg
Moran EV, Hartig F, Bell DM (2016) Intraspecific trait variation across scales: implications for understanding global change responses. Global Change Biology 22, 137–150.
| Intraspecific trait variation across scales: implications for understanding global change responses.Crossref | GoogleScholarGoogle Scholar | 26061811PubMed |
Morgan JW, Venn SE (2017) Alpine plant species have limited capacity for long-distance seed dispersal. Plant Ecology 218, 813–819.
| Alpine plant species have limited capacity for long-distance seed dispersal.Crossref | GoogleScholarGoogle Scholar |
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. Journal of Experimental Botany 64, 3983–3998.
| Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications.Crossref | GoogleScholarGoogle Scholar | 23913954PubMed |
New M, Lister D, Hulme M, Makin I (2002) A high-resolution data set of surface climate over global land areas. Climate Research 21, 1–25.
| A high-resolution data set of surface climate over global land areas.Crossref | GoogleScholarGoogle Scholar |
Nicholls N (2005) Climate variability, climate change and the Australian snow season. Australian Meteorological Magazine 54, 177–185.
Nicotra AB, Segal DL, Hoyle GL, Schrey AW, Verhoeven KJ, Richards CL (2015) Adaptive plasticity and epigenetic variation in response to warming in an alpine plant. Ecology and Evolution 5, 634–647.
| Adaptive plasticity and epigenetic variation in response to warming in an alpine plant.Crossref | GoogleScholarGoogle Scholar | 25691987PubMed |
Nogués-Bravo D, Araújo MB, Errea MP, Martínez-Rica JP (2007) Exposure of global mountain systems to climate warming during the 21st Century. Global Environmental Change 17, 420–428.
| Exposure of global mountain systems to climate warming during the 21st Century.Crossref | GoogleScholarGoogle Scholar |
Opedal OH, Armbruster WS, Graae BJ (2015) Linking small-scale topography with microclimate, plant species diversity and intra-specific trait variation in an alpine landscape. Plant Ecology & Diversity 8, 305–315.
| Linking small-scale topography with microclimate, plant species diversity and intra-specific trait variation in an alpine landscape.Crossref | GoogleScholarGoogle Scholar |
Osborne WS, Davis MS, Green K (1998) Temporal and spatial variation in snow cover. In ‘Snow. A natural history; an uncertain future’. (Ed. K Green) pp. 56–68. (Australian Alps Liaison Committee: Canberra)
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37, 637–669.
| Ecological and evolutionary responses to recent climate change.Crossref | GoogleScholarGoogle Scholar |
Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, et al. (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Piper FI, Fajardo A, Cavieres LA (2013) Simulated warming does not impair seedling survival and growth of Nothofagus pumilio in the southern Andes. Perspectives in Plant Ecology, Evolution and Systematics 15, 97–105.
| Simulated warming does not impair seedling survival and growth of Nothofagus pumilio in the southern Andes.Crossref | GoogleScholarGoogle Scholar |
Prevéy J, Vellend M, Rüger N, Hollister RD, Bjorkman AD, Myers‐Smith IH, Elmendorf SC, Clark K, Cooper EJ, Elberling B, et al. (2017) Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Global Change Biology 23, 2660–2671.
| Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes.Crossref | GoogleScholarGoogle Scholar | 28079308PubMed |
Randin CF, Engler R, Normand S, Zappa M, Zimmermann NE, Pearman PB, Vittoz P, Thuiller W, Guisan A (2009) Climate change and plant distribution: local models predict high-elevation persistence. Global Change Biology 15, 1557–1569.
| Climate change and plant distribution: local models predict high-elevation persistence.Crossref | GoogleScholarGoogle Scholar |
Richardson BA, Chaney L, Shaw NL, Still SM (2017) Will phenotypic plasticity affecting flowering phenology keep pace with climate change? Global Change Biology 23, 2499–2508.
| Will phenotypic plasticity affecting flowering phenology keep pace with climate change?Crossref | GoogleScholarGoogle Scholar | 27739159PubMed |
Rixen C, Dawes MA, Wipf S, Hagedorn F (2012) Evidence of enhanced freezing damage in treeline plants during six years of CO2 enrichment and soil warming. Oikos 121, 1532–1543.
| Evidence of enhanced freezing damage in treeline plants during six years of CO2 enrichment and soil warming.Crossref | GoogleScholarGoogle Scholar |
Rustad L, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562.
| A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming.Crossref | GoogleScholarGoogle Scholar | 28547240PubMed |
Scherrer D, Körner C (2010) Infra‐red thermometry of alpine landscapes challenges climatic warming projections. Global Change Biology 16, 2602–2613.
Scherrer D, Körner C (2011) Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. Journal of Biogeography 38, 406–416.
| Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming.Crossref | GoogleScholarGoogle Scholar |
Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17, 667–693.
| The evolution of phenotypic plasticity in plants.Crossref | GoogleScholarGoogle Scholar |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Sierra-Almeida A, Cavieres LA (2012) Summer freezing resistance of high-elevation plant species changes with ontogeny. Environmental and Experimental Botany 80, 10–15.
| Summer freezing resistance of high-elevation plant species changes with ontogeny.Crossref | GoogleScholarGoogle Scholar |
Sierra-Almeida A, Cavieres LA, Bravo LA (2009) Freezing resistance varies within the growing season and with elevation in high-Andean species of central Chile. New Phytologist 182, 461–469.
| Freezing resistance varies within the growing season and with elevation in high-Andean species of central Chile.Crossref | GoogleScholarGoogle Scholar | 19210722PubMed |
Taschler D, Neuner G (2004) Summer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary. Plant, Cell & Environment 27, 737–746.
| Summer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary.Crossref | GoogleScholarGoogle Scholar |
Therneau TM (2015) A package for survival analysis in S. ver. 2.38. Available at: https://CRAN.R-project.org/package=survival (accessed 7 January 2020).
Valladares F, Matesanz S, Guilhaumon F, Araújo MB, Balaguer L, Benito-Garzón M, Cornwell W, Gianolo E, van Kleunen M, Naya DE, Nicotra AB, Poorter H, Zavala MA (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters 17, 1351–1364.
| The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change.Crossref | GoogleScholarGoogle Scholar | 25205436PubMed |
van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist 166, 49–60.
| Constraints on the evolution of adaptive phenotypic plasticity in plants.Crossref | GoogleScholarGoogle Scholar | 15760350PubMed |
Venn SE, Morgan JW, Green PT (2009) Do facilitative interactions with neighboring plants assist the growth of seedlings at high altitudes in alpine Australia? Arctic, Antarctic, and Alpine Research 41, 381–387.
| Do facilitative interactions with neighboring plants assist the growth of seedlings at high altitudes in alpine Australia?Crossref | GoogleScholarGoogle Scholar |
Venn SE, Morgan JW, Lord JM (2013) Foliar freezing resistance of Australian alpine plants over the growing season. Austral Ecology 38, 152–161.
| Foliar freezing resistance of Australian alpine plants over the growing season.Crossref | GoogleScholarGoogle Scholar |
Vitasse Y, Hoch G, Randin C, Lenz A, Kollas C, Scheepens JF, Körner C (2013) Elevation adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171, 663–678.
| Elevation adaptation and plasticity in seedling phenology of temperate deciduous tree species.Crossref | GoogleScholarGoogle Scholar | 23306445PubMed |
Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011) Climate change and plant regeneration from seed. Global Change Biology 17, 2145–2161.
| Climate change and plant regeneration from seed.Crossref | GoogleScholarGoogle Scholar |
Wheeler JA, Hoch G, Cortes AJ, Sedlacek J, Wipf S, Rixen C (2014) Increased spring freezing vulnerability for alpine shrubs under early snowmelt. Oecologia 175, 219–229.
| Increased spring freezing vulnerability for alpine shrubs under early snowmelt.Crossref | GoogleScholarGoogle Scholar | 24435708PubMed |
Williams CM, Henry HA, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biological Reviews of the Cambridge Philosophical Society 90, 214–235.
| Cold truths: how winter drives responses of terrestrial organisms to climate change.Crossref | GoogleScholarGoogle Scholar | 24720862PubMed |
Wipf S, Stoeckli V, Bebi P (2009) Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Climatic Change 94, 105–121.
| Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing.Crossref | GoogleScholarGoogle Scholar |
Wisniewski M, Gusta L, Neuner G (2014) Adaptive mechanisms of freeze avoidance in plants: a brief update. Environmental and Experimental Botany 99, 133–140.
| Adaptive mechanisms of freeze avoidance in plants: a brief update.Crossref | GoogleScholarGoogle Scholar |
