Skip to main content
Log in

Does the life-history strategy determine the freezing resistance of flowers and leaves of alpine herbaceous species?

  • Original Article
  • Published:
Alpine Botany Aims and scope Submit manuscript

Abstract

In high-mountain habitats, summer frost events can have negative consequences for plant fitness. Despite this, most studies have evaluated the consequences of frosts for vegetative structures of perennial plants, and neither for leaves nor for flowers of annual plants. We hypothesize that the degree of freezing resistance of flowers and leaves of a species depends on its life-history strategy (LHS), and is probably the consequence of a trade-off between growth/reproduction and the cost of the freezing resistance. Specifically, flowers and leaves of short-lived annual species should be less freezing resistant than those of perennial plant species. We compared the freezing resistance of flowers and leaves of 10 annual and 12 perennial plant species from the Andes of central Chile using the electrolyte leakage method. Temperature damage for 50% tissue (LT50) of annual species was − 9.6 °C in flowers and − 11.9 °C in leaves. In perennial species, LT50 was similar in flowers (− 12.3 °C) and leaves (− 12.5 °C). Despite that, these differences were not significant (except the flowers of annual species), we found remarkable differences between LHS when freezing resistance was analyzed species by species. Like this, 58% and 83% of perennial species resist temperatures ≤ − 10 °C in their flowers and leaves, respectively, compared with only 30% and 40% of annual species. Additionally, in most of the species, the freezing resistance of leaves was greater than that of flowers, with this proportion being greater in annual (58%) than in perennial species (43%). Thus, we concluded that the degree of freezing resistance depends on the LHS, such that annual species, which are less freezing resistant than perennial species, have an infrequent occurrence and a distribution restricted to low elevation in high-mountain habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154:516–520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JL, Seeley SD (1993) Bloom delay in deciduous fruits. Hortic Rev 15:97–144

    Google Scholar 

  • Arias NS, Bucci SJ, Scholz FG, Goldstein G (2015) Freezing avoidance by supercooling in Olea europaea cultivars: the role of apoplastic water, solute content and cell wall rigidity. Plant Cell Environ 38:2061–2070

    CAS  PubMed  Google Scholar 

  • Arroyo MTK, Armesto JJ, Villagrán C (1981) Plant phenological patterns in the high Andean Cordillera of central Chile. J Ecol 69:205–223

    Google Scholar 

  • Arroyo MTK, Dudley LS, Jespersen G, Pacheco DA, Cavieres LA (2013) Temperature-driven flower longevity in a high-alpine species of Oxalis influences reproductive assurance. New Phytol 200:1260–1268

    PubMed  Google Scholar 

  • Ashman TL, Schoen DJ (1994) How long should flowers live? Nature 371:788–791

    CAS  Google Scholar 

  • Augspurger CK (2009) Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Funct Ecol 23:1031–1039

    Google Scholar 

  • Bannister P (2005) Frost resistance of the New Zealand narrow-leaved snow tussock grass, Chionochloa rigida. N Z J Bot 43:425–430

    Google Scholar 

  • Bazzaz FA, Morse FBS (1991) Annual plants: potential responses to multiple stresses. In: Mooney HA, Winner WE, Pell EJ (eds) Response of plants to multiple stresses. Academic Press, San Diego, pp 283–305

    Google Scholar 

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Google Scholar 

  • Billings WD (1974) Arctic and alpine vegetation: plant adaptations to cold summer climates. In: Ives JD, Barry RG (eds) Arctic and alpine environments. Methuen, London, pp 403–443

    Google Scholar 

  • Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529

    Google Scholar 

  • Bokhorst S, Bjerke JW, Bowles FW, Melillo J, Callaghan TV, Phoenix GK (2008) Impacts of extreme winter warming in the sub-Arctic: growing season responses of dwarf shrub heathland. Glob Chang Biol 14:2603–2612

    Google Scholar 

  • Bucher SF, Feiler R, Buchner O, Neuner G, Rosbakh S, Leiterer M, Römermann C (2019) Temporal and spatial trade-offs between resistance and performance traits in herbaceous plant species. Environ Exp Bot 157:187–196

    CAS  Google Scholar 

  • CaraDonna PJ, Bain JA (2016) Frost sensitivity of leaves and flowers of subalpine plants is related to tissue type and phenology. J Ecol 104:55–64

    Google Scholar 

  • Cavieres LA, Peñaloza A, Arroyo MTK (2000) Altitudinal vegetation belts in the high-Andes of Central Chile (33° S). Rev Chil Hist Nat 73:331–344

    Google Scholar 

  • Cavieres LA, Badano E, Sierra-Almeida A, Gómez-González S, Molina-Montenegro MA (2006) Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol 169:59–69

    PubMed  Google Scholar 

  • Cavieres LA, Badano E, Sierra-Almeida A, Molina-Montenegro MA (2007) Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the high Andes of central Chile. Arct Antarct Alp Res 39:229–236

    Google Scholar 

  • Chabot BF, Billings WD (1972) Origins and ecology of the Sierran alpine flora and vegetation. Ecol Monogr 42:163–199

    Google Scholar 

  • Díaz S, Hodgson JG, Thompson K et al (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304

    Google Scholar 

  • Diemer M (1998) Life span and dynamics of leaves of herbaceous perennials in high-elevation environments: ‘news from the elephant’s leg’. Funct Ecol 12:413–425

    Google Scholar 

  • Dumlao MR, Darehshouri A, Cohu CM, Muller O, Mathias J, Adams WW III, Demmig-Adams B (2012) Low temperature acclimation of photosynthetic capacity and leaf morphology in the context of phloem loading type. Photosyn Res 113:81–189

    Google Scholar 

  • Garnier E (1992) Growth analysis of congeneric annual and perennial grass species. J Ecol 80:665–675

    Google 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. J Veg Sci 24:569–579

    Google Scholar 

  • Hacker J, Ladinig U, Wagner J, Neuner G (2011) Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling. Plant Sci 180:149–156

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hancock JF, Pritts MP (1987) Does reproductive effort vary across different life forms and seral environments? A review of the literature. Bull Torrey Bot Club 114:53–59

    Google Scholar 

  • Hoffmann A, Arroyo MTK, Liberona F, Muñoz M, Watson J (1998) Plantas Altoandinas en la Flora Silvestre de Chile. Ediciones Fundación Claudio Gay, Santiago

    Google Scholar 

  • Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3:457–463

    Google Scholar 

  • Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362

    PubMed  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems; with 47 tables, 2nd edn. Springer-Verlag, Berlin

    Google Scholar 

  • Körner C, Alsos IG (2009) Freezing resistance in high arctic plant species of Svalbard in mid-summer. Bauhinia 21:25–32

    Google Scholar 

  • Körner C, Renhardt U (1987) Dry matter partitioning and root length/leaf area ratios in herbaceous perennial plants with diverse altitudinal distribution. Oecologia 74:411–418

    PubMed  Google Scholar 

  • Ladinig U, Hacker J, Neuner G, Wagner J (2013) How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia 171:743–760

    PubMed  PubMed Central  Google Scholar 

  • Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional groups. Springer Science and Business Media, Berlin

    Google Scholar 

  • Larcher W, Kainmüller C, Wagner J (2010) Survival types of high mountain plants under extreme temperatures. Flora 205:3–18

    Google Scholar 

  • Lenz A, Hoch G, Vitasse Y, Körner C (2013) European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients. New Phytol 200:1166–1175

    PubMed  Google Scholar 

  • Lipp CC, Goldstein G, Meinzer FC, Niemczura W (1994) Freezing tolerance and avoidance in high-elevation Hawaiian plants. Plant Cell Environ 17:1035–1044

    Google Scholar 

  • Loik ME, Still C, Huxman T, Harte J (2004) In situ photosynthetic freezing tolerance for plants exposed to a global warming manipulation in the Rocky Mountains, Colorado, USA. New Phytol 162:331–341

    Google Scholar 

  • Lu S, Rieger M (1993) Effect of temperature preconditioning on ovary freezing tolerance of fully opened peach flowers. J Hortic Sci 68:343–347

    Google Scholar 

  • Neuner G, Beikircher B (2010) Critically reduced frost resistance of Picea abies during sprouting could be linked to cytological changes. Protoplasma 243:145–152

    CAS  PubMed  Google Scholar 

  • Neuner G, Erler A, Ladinig U, Hacker J, Wagner J (2013) Frost resistance of reproductive tissues during various stages of development in high mountain plants. Physiol Plant 147:88–100

    CAS  PubMed  Google Scholar 

  • Pacheco DA, Dudley LS, Cabezas J, Cavieres LA, Arroyo MTK (2016) Plastic responses contribute to explaining altitudinal and temporal variation in potential flower longevity in high Andean Rhodolirion montanum. PLoS ONE 11:e0166350. https://doi.org/10.1371/journal.pone.0166350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pescador DS, Sierra-Almeida A, Torres PJ, Escudero A (2016) Summer freezing resistance: a critical filter for plant community assemblies in Mediterranean High-mountains. Front Plant Sci 7:197. https://doi.org/10.3389/fpls.2016.00194

    Article  Google Scholar 

  • Proebsting EL, Mills HH (1978) A synoptic analysis of peach and cherry bud hardiness. J Am Soc Hortic Sci 103:842–845

    Google Scholar 

  • Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Google Scholar 

  • 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

    Google Scholar 

  • Rodrigo J (2000) Spring frosts in deciduous fruit trees —morphological damage and flower hardiness. Sci Hortic 85:155–173

    Google Scholar 

  • Rodríguez R, Marticorena C, Alarcón D et al (2018) Catalogue of the vascular plants of Chile. Gayana Bot 75:1–430

    Google Scholar 

  • Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress. Springer-Verlag, Berlin

    Google Scholar 

  • Sakai A, Otsuka K (1970) Freezing resistance of alpine plants. Ecology 51:665–671

    Google Scholar 

  • Santibañez F, Uribe J (1990) Atlas Agroclimático de Chile. Regiones V y Metropolitana. Universidad de Chile, Facultad de Ciencias Agrarias y Forestales, Santiago

    Google Scholar 

  • Sierra-Almeida A, Cavieres LA (2012) Summer freezing resistance of high-elevation plant species changes with ontogeny. Environ Exp Bot 80:10–15

    Google Scholar 

  • Sierra-Almeida A, Cavieres LA, Bravo LA (2009) Freezing resistance varies within the growing season and with the elevation in high-Andean species of central Chile. New Phytol 182:461–469

    PubMed  Google Scholar 

  • Sierra-Almeida A, Cavieres LA, Bravo LA (2010) Freezing resistance of high elevation plant species is not related to their height or growth-form in the central Chilean Andes. Environ Exp Bot 69:273–278

    Google Scholar 

  • Sierra-Almeida A, Reyes-Bahamonde C, Cavieres LA (2016) Drought increases the freezing resistance of high-elevation plants of the central Chilean Andes. Oecologia 181:1011–1023

    PubMed  Google Scholar 

  • Sklenář P, Kucerova A, Macek P, Mackova J (2010) Does plant height determine the freezing resistance in the páramo plants? Austral Ecol 35:929–934

    Google Scholar 

  • Squeo FA, Rada F, García C, Ponce M, Rojas A, Azócar A (1996) Cold resistance mechanisms in high desert Andean plants. Oecologia 105:552–555

    PubMed  Google Scholar 

  • Stead AD, Van Doorn WG, Jones ML, Wagstaff C (2008) Flower senescence: fundamental and applied aspects. In: Ainsworth C (ed) Annual plant reviews, flowering and its manipulation. Blackwell Publishing Ltd, Oxford, pp 261–296

    Google Scholar 

  • 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 Environ 27:737–746

    Google Scholar 

  • Teillier S, Marticorena A, Niemeyer HM (2011) Flora Altoandina de Santiago. Guía para la identificación de las especies de las cuencas del Maipo y del Mapocho. Universidad de Chile, Santiago.

  • Torres-Díaz C, Gómez-González S, Stotz GC, Torres-Morales P, Paredes B, Pérez-Millaqueo M, Gianoli E (2011) Extremely long-lived stigmas allow extended cross-pollination opportunities in a High Andean plant. PLoS ONE 6:e19497. https://doi.org/10.1371/journal.pone.0019497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venn SE, Morgan JW, Lord JM (2013) Foliar freezing resistance of Australian alpine plants over the growing season. Austral Ecol 38:152–161

    Google Scholar 

  • Vitasse Y, Lenz A, Körner C (2014) The interaction between freezing tolerance and phenology in temperate deciduous trees. Front Plant Sci 5:541. https://doi.org/10.3389/fpls.2014.00541

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilner J (1960) Relative and absolute electrolytic conductance tests for frost hardiness of apple varieties. Can J Plant Sci 40:630–637

    Google Scholar 

  • Wingler A (2015) Comparison of signalling interactions determining annual and perennial plant growth in response to low temperature. Front Plant Sci 5:794. https://doi.org/10.3389/fpls.2014.00794

    Article  PubMed  PubMed Central  Google Scholar 

  • Woodward FI (1987) Climate and plant distribution. Cambridge University Press, Cambridge

    Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    CAS  PubMed  Google Scholar 

  • Zhang YJ, Bucci SJ, Arias NS, Scholz FG, Hao GY, Cao KF, Goldstein G (2016) Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size. Tree Physiol 36:1007–1018

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank Omar, Octavia, and Bárbara for their help in the fieldwork, Alicia Marticorena and MAK Mihŏc for plant identifications, and Daniel Harris-Pascal for English edition of the manuscript.

Funding

This work was supported by The National Commission for Science and Technology (CONICYT) through the National Fund for Scientific and Technological Development (FONDECYT 11150710 (AS-A) and FONDECYT 1181688 (AS), and Doctoral Fellowship CONICYT 21151063 (LVM).

Author information

Authors and Affiliations

Authors

Contributions

LVM and AS-A conceived and designed the research; LVM, CAC and CS carried out the collection and data analysis. LVM interpreted the results and wrote the manuscript with support from AS-A and AS.

Corresponding author

Correspondence to Loreto V. Morales.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study does not involve research on human participants or animals.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 36 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morales, L.V., Alvear, C., Sanfuentes, C. et al. Does the life-history strategy determine the freezing resistance of flowers and leaves of alpine herbaceous species?. Alp Botany 130, 157–168 (2020). https://doi.org/10.1007/s00035-020-00236-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00035-020-00236-5

Keywords

Navigation