Seedling mortality during biphasic drought in sandy Mediterranean soils
Stephen M. Benigno A B , Kingsley W. Dixon A B and Jason C. Stevens A B C
+ Author Affiliations
- Author Affiliations
A Botanic Gardens and Parks Authority, Science Directorate, West Perth, WA 6005, Australia.
B The University of Western Australia, School of Plant Biology, Crawley, WA 6009, Australia.
C Corresponding author. Email: jason.stevens@bgpa.wa.gov.au
Functional Plant Biology 41(12) 1239-1248 https://doi.org/10.1071/FP13366
Submitted: 20 December 2013 Accepted: 26 May 2014 Published: 14 August 2014
Abstract
Climate change is increasing the frequency and intensity of drought, and seedling response to a recurrent pattern of drought stress is necessary to understand vegetation establishment patterns in particularly for ecological restoration and conservation projects. A controlled environment study investigated seedling physiological response of framework Mediterranean tree species to simulated successive droughts. Six-month-old seedlings were grown in 1.0 m tall pots to emulate deep soil profiles and subjected to a well watered treatment and a drought treatment consisting of an initial 60 day drought (water withholding), followed by 120 days of re-watering and a subsequent 60 day drought. Soil water access, soil water content, maximum root depth and xylem water potential were assessed through successive harvests. To assess seedling response to multiple droughts, gas-exchange and chlorophyll fluorescence measurements were taken every 15 days after each drought, and multiple times throughout re-watering. No seedling mortality was observed during the initial drought, whereas 100% mortality of all species occurred within 48 days of the second drought. Seedling gas exchange and water potential decreased with decreasing water availability but was dependent on the isohydric or anisohydric behaviour of individual species. An absence of sustained photoprotection during the second drought phase heightened photodamage to foliar tissues resulting in a more rapid decrease of gs and leaf water potential. Therefore, biphasic drought proved detrimental to seedling establishment by reducing physiological resilience, highlighting the severity of future climate change predictions towards the regeneration capacity of Mediterranean ecosystems.
Additional keywords: biodiversity hotspot, drought recovery, drought stress, physiological tolerance, seedling establishment.
References
Beis A, Patakas A (2010) Differences in stomatal responses and root to shoot signalling between two grapevine varieties subjected to drought. Functional Plant Biology 37, 139–146.| Differences in stomatal responses and root to shoot signalling between two grapevine varieties subjected to drought.Crossref | GoogleScholarGoogle Scholar |
Black C (1965) ‘Methods of soil analysis. Part 1: Physical and mineralogical properties.’ (American Society of Agronomy Inc., Madison, WI, USA)
Cochard H, Coll L, Le Roux X, Améglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiology 128, 282–290.
| Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVSqtw%3D%3D&md5=46eb43ce98688e317ba2dc89426629b6CAS | 11788773PubMed |
Dodd J, Heddle EM, Pate JS, Dixon KW (1984) Rooting patterns of sandplain plants and their functional significance. In ‘Kwongan, plant life of the sandplain: biology of a south-west Australian shrubland ecosystem’. (Eds JS Pate, JS Bear) pp. 146–177. (UWA Press: Perth)
Epron D, Dreyer E (1993) Long-term effects of drought on photosynthesis of adult oak trees (Quercus petraea (Matt.) Liebl. and Quercus robur L.) in a natural stand. New Phytologist 125, 381–389.
| Long-term effects of drought on photosynthesis of adult oak trees (Quercus petraea (Matt.) Liebl. and Quercus robur L.) in a natural stand.Crossref | GoogleScholarGoogle Scholar |
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S, Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (2009) ‘Plant drought stress: effects, mechanisms and management, sustainable agriculture.’ (Springer: Dordrecht, The Netherlands)
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33, 317–345.
| Stomatal conductance and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=3a73a520dccb5d008b17264757da14c1CAS |
Flexas J, Medrano H (2002) Drought‐inhibition of photosynthesis in C3 plants. Stomatal and Non-stomatal Limitations Revisited. Annals of Botany 89, 183–189.
Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343–352.
| Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhu7o%3D&md5=d285770523d464463fb48e72249a065bCAS |
Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant, Cell & Environment 30, 19–30.
| Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance.Crossref | GoogleScholarGoogle Scholar |
Gallé A, Feller U (2007) Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery. Physiologia Plantarum 131, 412–421.
| Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery.Crossref | GoogleScholarGoogle Scholar | 18251880PubMed |
Gallé A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytologist 174, 799–810.
| Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery.Crossref | GoogleScholarGoogle Scholar | 17504463PubMed |
Galle A, Florez-Sarasa I, Tomas M, Pou A, Medrano H, Ribas-Carbo M, Flexas J (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? Journal of Experimental Botany 60, 2379–2390.
| The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyiur8%3D&md5=09bd7252eb490a799a4ce374acb9a62dCAS | 19321646PubMed |
Galle A, Florez-Sarasa I, Aououad HE, Flexas J (2011) The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles. Journal of Experimental Botany 62, 5207–5216.
| The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejsrbJ&md5=837baba7ea72c93191ecf55986efb30eCAS | 21813795PubMed |
Galmés J, Medrano H, Flexas J (2007a) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 175, 81–93.
| Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms.Crossref | GoogleScholarGoogle Scholar | 17547669PubMed |
Galmés J, Flexas J, Savé R, Medrano H (2007b) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant and Soil 290, 139–155.
| Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery.Crossref | GoogleScholarGoogle Scholar |
Galmés J, Abadía A Cifre J, Medrano H, Flexas J (2007c) Photoprotection processes under water stress and recovery in Mediterranean plants with different growth forms and leaf habits. Physiologia Plantarum 130, 495–510.
| Photoprotection processes under water stress and recovery in Mediterranean plants with different growth forms and leaf habits.Crossref | GoogleScholarGoogle Scholar |
Gebrekirstos A, Teketay D, Fetene M, Mitlöhner R (2006) Adaptation of five co-occurring tree and shrub species to water stress and its implication in restoration of degraded lands. Forest Ecology and Management 229, 259–267.
| Adaptation of five co-occurring tree and shrub species to water stress and its implication in restoration of degraded lands.Crossref | GoogleScholarGoogle Scholar |
Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA (2001) Cavitation fatigue embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiology 125, 779–786.
| Cavitation fatigue embolism and refilling cycles can weaken the cavitation resistance of xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhs1Klsb8%3D&md5=9b91ba8864968836d24731ebbe30c0a2CAS | 11161035PubMed |
Halvorson WL, Patten DT (1974) Seasonal water potential changes in Sonoran Desert shrubs in relation to topography. Ecology 55, 173–177.
| Seasonal water potential changes in Sonoran Desert shrubs in relation to topography.Crossref | GoogleScholarGoogle Scholar |
Hazelton P, Murphy B (2007) ‘What do all the numbers mean? A guide for the interpretation of soil test results.’ (CSIRO Publishing: Melbourne)
Holmgren M, Scheffer M (2001) El Niño as a window of opportunity for the restoration of degraded arid ecosystems. Ecosystems 4, 151–159.
| El Niño as a window of opportunity for the restoration of degraded arid ecosystems.Crossref | GoogleScholarGoogle Scholar |
Kitao M, Lei TT, Koike T, Tobita H, Maruyama Y (2003) Higher electron transport rate observed at low intercellular CO2 concentration in long-term drought-acclimated leaves of Japanese mountain birch (Betula ermanii). Physiologia Plantarum 118, 406–413.
| Higher electron transport rate observed at low intercellular CO2 concentration in long-term drought-acclimated leaves of Japanese mountain birch (Betula ermanii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVSisLs%3D&md5=53820e3a6cfcca94b9a23042312d74f2CAS |
Landis T, Tinus R, Barnett J (1998) ‘The container tree nursery manual. USDA Agricultural Handbook 674. Seedling propagation.’ (USDA Forest Service, Washington, DC)
Liu C-C, Liu Y-G, Guo K, Zheng Y-R, Li G-Q, Yu L-F, Yang R (2010) Influence of drought intensity on the response of six woody karst species subjected to successive cycles of drought and rewatering. Physiologia Plantarum 139, 39–54.
| Influence of drought intensity on the response of six woody karst species subjected to successive cycles of drought and rewatering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtVWnsbc%3D&md5=37803afe8a7c01d384f2e0c9d3d05378CAS | 20059730PubMed |
Lloret F, Siscart D, Dalmases C (2004) Canopy recovery after drought dieback in holm-oak Mediterranean forests of Catalonia (NE Spain). Global Change Biology 10, 2092–2099.
| Canopy recovery after drought dieback in holm-oak Mediterranean forests of Catalonia (NE Spain).Crossref | GoogleScholarGoogle Scholar |
Lo Gullo MA, Salleo S (1988) Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. New Phytologist 108, 267–276.
| Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions.Crossref | GoogleScholarGoogle Scholar |
McArthur W (1991) ‘Reference soils of south-western Australia.’ (WA Department of Agriculture: Perth)
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178, 719–739.
| Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?Crossref | GoogleScholarGoogle Scholar | 18422905PubMed |
Miyashita K, Tanakamaru S, Maitani T, Kimura K (2005) Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environmental and Experimental Botany 53, 205–214.
| Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVyksrk%3D&md5=67f2615ebda1d15a6ed9d56963b1220dCAS |
Mueller RC, Scudder CM, Porter ME, Talbot Trotter R, Gehring CA, Whitham TG (2005) Differential tree mortality in response to severe drought: evidence for long-term vegetation shifts. Journal of Ecology 93, 1085–1093.
| Differential tree mortality in response to severe drought: evidence for long-term vegetation shifts.Crossref | GoogleScholarGoogle Scholar |
Poot P, Lambers H (2003) Growth responses to waterlogging and drainage of woody Hakea (Proteaceae) seedlings, originating from contrasting habitats in south-western Australia. Plant and Soil 253, 57–70.
| Growth responses to waterlogging and drainage of woody Hakea (Proteaceae) seedlings, originating from contrasting habitats in south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsLY%3D&md5=ca164026de2da64f73a86a94d4d45ed6CAS |
Quick WP, Chaves MM, Wendler R, David M, Rodrigues ML, Passaharinho JA, Pereira JS, Adcock MD, Leegood RC, Stitt M (1992) The effect of water stress on photosynthetic carbon metabolism in four species grown under field conditions. Plant, Cell & Environment 15, 25–35.
| The effect of water stress on photosynthetic carbon metabolism in four species grown under field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XisFaitbo%3D&md5=6aeebef0b92e503ab1338d7cf10b9d94CAS |
Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany 82, 222–237.
| Rapid light curves: a powerful tool to assess photosynthetic activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslylsb0%3D&md5=325fe5489bd6f3403e1a1cc48b148b32CAS |
Rokich D (1999) ‘Restoration of a Banksia woodland following sand extraction.’ (University of Western Australia: Perth)
Salama R, Silberstein R, Pollock D (2005) Soils characteristics of the Bassendean and Spearwood Sands of the Gnangara Mound (Western Australia) and their controls on recharge, water level patterns and solutes of the superficial aquifer. Water, Air, & Soil Pollution: Focus 5, 3–26.
| Soils characteristics of the Bassendean and Spearwood Sands of the Gnangara Mound (Western Australia) and their controls on recharge, water level patterns and solutes of the superficial aquifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlejt7k%3D&md5=c3a32ad40c1bdbfa44d44489200de788CAS |
Sánchez-Gómez D, Valladares F, Zavala MA (2006) Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytologist 170, 795–806.
| Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation.Crossref | GoogleScholarGoogle Scholar | 16684239PubMed |
Schär C, Vidale PL, Lüthi D, Frei C, Häberli C, Liniger MA, Appenzeller C (2004) The role of increasing temperature variability in European summer heatwaves. Nature 427, 332–336.
| The role of increasing temperature variability in European summer heatwaves.Crossref | GoogleScholarGoogle Scholar | 14716318PubMed |
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413, 591–596.
| Catastrophic shifts in ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsleht7c%3D&md5=1609fe49c0258b5233e2d7156c6c69afCAS | 11595939PubMed |
Sitters J, Holmgren M, Stoorvogel JJ, López BC (2012) Rainfall-tuned management facilitates dry forest recovery. Restoration Ecology 20, 33–42.
| Rainfall-tuned management facilitates dry forest recovery.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Pockman WT (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant, Cell & Environment 16, 279–287.
| Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis.Crossref | GoogleScholarGoogle Scholar |
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419–432.
| Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours.Crossref | GoogleScholarGoogle Scholar |
Turner N (1988) Measurement of plant water status by the pressure chamber technique. Irrigation Science 9, 289–308.
| Measurement of plant water status by the pressure chamber technique.Crossref | GoogleScholarGoogle Scholar |
Veneklaas E, Poot P (2003) Seasonal patterns in water use and leaf turnover of different plant functional types in a species-rich woodland, south-western Australia. Plant and Soil 257, 295–304.
| Seasonal patterns in water use and leaf turnover of different plant functional types in a species-rich woodland, south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslWrt74%3D&md5=2fa3a4a0715cfafd93bd724562f211a6CAS |
Vilagrosa A, Cortina J, Gil-Pelegrín E, Bellot J (2003) Suitability of drought-preconditioning techniques in Mediterranean climate restoration. Ecology 11, 208–216.
von Caemmerer S (2000) ‘Biochemical models of leaf photosynthesis. Techniques in plant sciences.’ (CSIRO Publishing: Melbourne)
Walter J, Nagy L, Hein R, Rascher U, Beierkuhnlein C, Willner E, Jentsch A (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environmental and Experimental Botany 71, 34–40.
| Do plants remember drought? Hints towards a drought-memory in grasses.Crossref | GoogleScholarGoogle Scholar |
Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kumar D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson LT, van Zyl L, Egertsdotter U, Sederoff RR, Grene R (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiology 133, 1702–1716.
| Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFCh&md5=6d446d5b1071aad4737248f614193b51CAS | 14681533PubMed |
Xu Z, Zhou G, Shimizu H (2009) Are plant growth and photosynthesis limited by pre-drought following rewatering in grass? Journal of Experimental Botany 60, 3737–3749.
| Are plant growth and photosynthesis limited by pre-drought following rewatering in grass?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2ks7%2FK&md5=03d43f515874aff9d92973ad801d369cCAS | 19596698PubMed |
Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38, 171–186.
| Plant responses to drought, acclimation, and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVehtr8%3D&md5=93e6ae782cb64b813509181d6a3985f7CAS |
