Abstract
Key message
Desert woody species demonstrated a high morphological plasticity to water. This would allow them to use increased rainfall predicted by climate change, but might challenge the drought resistance of irrigated nursery-produced plants for revegetation.
Abstract
Phenotypic plasticity is the ability of a given genotype to produce different phenotypes in response to changing environmental conditions. Despite its high adaptive value, it may have a high cost in resource-poor ecosystems, restricting the ability of plants to take advantage of surplus resources, e.g., increased levels of precipitation. We aimed to determine the phenotypic plasticity to water availability of four woody species from a hot desert of South America. We carried out a pot experiment with two levels of irrigation in a glasshouse, where performance (biomass production, stem growth, survival) and functional traits (biomass allocation, total leaf area, leaf size, specific leaf area; stomata size, density and index; photoprotective and antioxidant compounds) were measured. The plasticity patterns differed between species, with the highest plasticity in leaf traits (around 80% change between treatments), and the lowest in biochemical traits (no significant variation between treatments). All four species increased their performance under high-water supply, with different magnitudes (the two phreatophytes > the two xerophytes). However, some of them showed increased allocation to stem biomass, increased total leaf area and leaf size, increased stomata size, and reduced root growth, potentially allowing them to use water for growth when it is available, although hampering their drought resistance, based on classic interpretation of traits’ adaptive value. These changes promoted in irrigated nursery-produced seedlings should be considered in dryland revegetation plans. Moreover, our results suggest that the patterns of phenotypic plasticity would not be associated with the functional group of the species in relation to access of the water table in the field, but this issue needs to be explored further.
Similar content being viewed by others
Data availability
The data that support this study will be shared upon reasonable request to the corresponding author.
References
Álvarez JA, Villagra PE (2009) Prosopis flexuosa DC. (Fabaceae, Mimosoideae). Kurtziana 35:49–63
Alpert P, Simms EL (2002) The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust? Evol Ecol 16:285–297
Baythavong BS, Stanton ML (2010) Characterizing selection on phenotypic plasticity in response to natural environmental heterogeneity. Evolution 64:2904–2920
Berli FJ, Alonso R, Bressan-Smith R, Bottini R (2013) UV-B impairs growth and gas exchange in grapevines grown in high altitude. Phys Plant 149:127–140
Biruk LN (2021) Ecofisiología de especies leñosas del Monte Central: aportes para la selección de especies y métodos de cultivo para la restauración de tierras secas. Tesis Doctoral, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, p 166
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Advances in genetics, vol 13. Academic Press, pp 115–155
Carvajal DE, Loayza AP, Ríos RS, Gianoli E, Squeo FA (2017) Population variation in drought-resistance strategies in a desert shrub along an aridity gradient: interplay between phenotypic plasticity and ecotypic differentiation. Perspect Plant Ecol Evol Syst 29:12–19
Chapelle EW, Kim MS, Mc Murtrey J (1992) Ratio analysis of reflectance spectra (RARS): an algorithm for the remote estimation of the concentration of chlorophyll a, chlorophyll b, and carotenoids in soybean leaves. Remote Sens Environ 39:239–247
Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Phys Biochem 72:1–20
Cortina J, Green JJ, Baddeley JA, Watson CA (2008) Root morphology and water transport of Pistacia lentiscus seedlings under contrasting water supply: a test of the pipe stem theory. Environ Exp Bot 62:343–350
Cortina J, Vilagrosa A, Trubat R (2013) The role of nutrients for improving seedling quality in drylands. New for 44:719–732
Couso LL, Fernández RJ (2012) Phenotypic plasticity as an index of drought tolerance in three Patagonian steppe grasses. Ann Bot 110:849–857
Cowie AL, Penman TD, Gorissen L, Winslow MD, Lehmann J, Tyrrell TD, Twomlow S, Wilkes A, Lal R, Jones JW, Paulsch A, Kellner K, Akhtar-Schuster M (2011) Towards sustainable land management in the drylands: scientific connections in monitoring and assessing dryland degradation, climate change and biodiversity. Land Degrad Dev 22:248–260
de Witt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. TREE 3:77–81
del Campo AD, Navarro RM, Ceacero CJ (2010) Seedling quality and field performance of commercial stocklots of containerized holm oak (Quercus ilex) in Mediterranean Spain: an approach for establishing a quality standard. New for 39:19–37
Dow GJ, Bergmann DC (2014) Patterning and processes: how stomatal development defines physiological potential. Curr Opin Plant Biol 21:67–74
Funk J (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173
Gianoli E, González-Teuber M (2005) Environmental heterogeneity and population differentiation in plasticity to drought in Convolvulus chilensis (Convolvulaceae). Evol Ecol 19:603–613
Giordano CV, Guevara A, Boccalandro HE, Sartor C, Villagra PE (2011) Water status, drought responses, and growth of Prosopis flexuosa trees with different access to the water table in a warm South American desert. Plant Ecol 212:1123–1134
Givinish TJ (2002) Ecological constraints on the evolution of plasticity in plants. Evol Ecol 16(213–242):2002
Goirán S, Aranibar JN, Gomez ML (2012) Heterogeneous spatial distribution of traditional livestock settlements and their effects on vegetation cover in arid groundwater coupled ecosystems in the Monte desert (Argentina). J Arid Environ 87:188–197
González CV, Jofré MF, Vila H, Stoffel M, Bottini R, Giordano CV (2016) Morphology and hydraulic architecture of Vitis vinifera L. cv. Syrah and Torrontés Riojano plants are unaffected by variations in Red to Far-Red Ratio. PLoS ONE 11(12):e0167767. https://doi.org/10.1371/journal.pone.0167767
Grant OM, Incoll LD, McNeilly T (2015) Variation in growth responses to availability of water in Cistus albidus populations from different habitats. Funct Plant Biol 32:817–829
Guevara A, Giordano CV (2015) Hydrotropism in lateral but not in pivotal roots of desert plant species under simulated natural conditions. Plant Soil 389:257–272
Guevara A, Pancotto V, Mastrantonio L, Giordano CV (2018) Fine roots of Prosopis flexuosa trees in the field. Plant and soil variables that control their growth and depth distribution. Plant Ecol 219:1399–1412
Holmgren M, Scheffer M (2001) El Niño as a window of opportunity for the restoration of degraded arid ecosystems. Ecosystems 4:151–159
Holmgren M, Stapp P, Dickman CR, Gracía C, Graham S, Gutiérrez JR, Hic C, Jaksic F, Kelt DA, Letnic M, Lima M, López BC, Meserve PL, Milstead WB, Poli GA, Previtali MA, Richter M, Sabaté S, Squeo FA (2006) A synthesis of ENSO effects on drylands in Australia, North America and South America. Adv Geosci 6:69–72
Jobbágy EG, Nosetto MD, Villagra PE, Jackson RB (2011) Water subsidies from mountains to deserts: their role in sustaining groundwater-fed oases in a sandy landscape. Ecol Appl 21:678–694
Labraga JC, Villalba R (2009) Climate in the Monte Desert: past trends, present conditions, and future projections. J Arid Environ 73:154–163
Lázaro-Nogal A, Matesanz S, Godoy A, Pérez-Trautman F, Gianoli E, Valladares F (2015) Environmental heterogeneity leads to higher plasticity in dry-edge populations of a semi-arid Chilean shrub: insights into climate change responses. J Ecol 103:338–350
Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci 1206:35–55
Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Phys 122:117–126
Meglioli PA, Riveros C, Villagra PE (2012) Biología de especies australes: Prosopis argentina Burkart (Fabaceae, Mimosoideae). Kurtziana 37(2):49–58
Meglioli PA, Aranibar JN, Villagra PE, Riveros CV (2017) Spatial patterns of soil resources under different land use in Prosopis woodlands of the Monte desert. CATENA 149:86–97
Molina-Montenegro MA, Atala C, Gianoli E (2010) Phenotypic plasticity and performance of Taraxacum officinale (dandelion) in habitats of contrasting environmental heterogeneity. Biol Invasions 12:2277–2284
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50
Qaderi MM, Cavers PB, Bernards MA (2002) Seed bank dynamics of Onopordum acanthium: emergence patterns and chemical attributes. J Ecol 90:672–683
Qi X, Torii KU (2018) Hormonal and environmental signals guiding stomatal development. BMC Biol 16:1–11
Ramírez-Valiente JA, Sánchez-Gómez D, Aranda I, Valladares F (2010) Phenotypic plasticity and local adaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different water availabilities. Tree Phys 30:618–627
Reed TE, Waples RS, Schindler DE, Hard JJ, Kinnison MT (2010) Phenotypic plasticity and population viability: the importance of environmental predictability. Proc R Soc Lond, B 277:3391–3400
Reynolds HL, D’Antonio C (1996) The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion. Plant Soil 185:75–97
Salazar PC, Navarro-Cerrillo RM, Cruz G, Grados N, Villar R (2019) Variability in growth and biomass allocation and the phenotypic plasticity of seven Prosopis pallida populations in response to water availability. Trees 33:1409–1422
Sánchez-Gómez D, Zavala MA, Valladares F (2008) Functional traits and plasticity linked to seedlings’ performance under shade and drought in Mediterranean woody species. Ann for Sci 65:311
Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Evol Syst 17:667–693
Scholander PF, Bradstreet ED, Hemmingsen EA, Hammel HT (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148:339–346
Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B (2019) Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 24:2452
Solé-Medina A, Robledo-Arnuncio JJ, Ramírez-Valiente JA (2022) Multi-trait genetic variation in resource-use strategies and phenotypic plasticity correlates with local climate across the range of a Mediterranean oak (Quercus faginea). New Phyt 234:462–478
Valladares F, Wright J, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936
Valladares F, Sánchez-Gómez D, Zavala M (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116
Valliere JM, Zhang J, Sharifi MR, Rundel PW (2019) Can we condition native plants to increase drought tolerance and improve restoration success? Ecol Appl 29:e01863
van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60
Velikova V, Arena A, Izzo LG, Tsonev T, Koleva D, Tattini M, Roeva O, De Maio A, Loreto F (2020) Functional and structural leaf plasticity determine photosynthetic performances during drought stress and recovery in two Platanus orientalis populations from contrasting habitats. Int J Mol Sci 21:3912. https://doi.org/10.3390/ijms21113912
Vilela AE, González-Paleo L (2015) Changes in resource-use strategy and phenotypic plasticity associated with selection for yield in wild species native to arid environments. J Arid Environ 113:51–58
Vilela AE, Agüero PR, Ravetta DA, González-Paleo L (2012) Long-term plasticity in growth, storage and defence allocation produces drought-tolerant juvenile shrubs of Prosopis alpataco R. A. Philippi (Fabaceae) Flora—morphology, distribution. Funct Ecol Plants 207:436–441
Villagra PE, Roig FA (2002) Distribución geográfica y fitosociológica de Prosopis argentina y P. alpataco (Fabaceae, Mimosideae). Bol Soc Argent Bot 37:1–8
Villagra PE, Defossé GE, Del Valle HF, Tabeni S, Rostagno M, Cesca E, Abraham E (2009) Land use and disturbance effects on the dynamics of natural ecosystems of the Monte Desert: implications for their management. J Arid Environ 73:202–211
Villar-Salvador P, Penelles R, Oliet J, Peñuelas JL, Jacobbs DF, González M (2004) Drought tolerance and transplanting performance of holm oak (Quercus ilex) seedlings after drought hardening in the nursery. Tree Phys 24:1147–1155
Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Phys 144:307–313
Acknowledgements
We thank Cornejo Ayelén, Debandi Hugo, Frete Juan, Gazaléz Gabriela, Giuffre Nicolás, Zalazar Gabriel and Zalazar Gualberto for their invaluable help in maintaining the experimental trial and carrying out the measurements.
Funding
This study was funded by the “Agencia Nacional de Promoción Científica y Tecnológica” of Argentina (PICT 2011-2521) to Giordano C. V., and by the Universidad Nacional de Cuyo (06/P31) to González C. V.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Communicated by Sergio Rossi.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Biruk, L.N., Fernández, M.E., González, C.V. et al. High and diverse plastic responses to water availability in four desert woody species of South America. Trees 36, 1881–1894 (2022). https://doi.org/10.1007/s00468-022-02335-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-022-02335-8