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Dry-forest tree species with large seeds and low stem specific density show greater survival under drought

Published online by Cambridge University Press:  26 January 2019

Lalitha Krishnan*
Affiliation:
National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research (TIFR), Bangalore 560065, India
Deepak Barua
Affiliation:
Department of Biology, Indian Institute of Science Education and Research (IISER), Pune 411008, India
Mahesh Sankaran
Affiliation:
National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research (TIFR), Bangalore 560065, India School of Biology, University of Leeds, Leeds LS2 9JT, UK

Abstract

Tree establishment in tropical dry forests is constrained by drought-related seedling mortality during early stages of recruitment. Predicted increases in the duration of growing-season droughts in the future pose a significant threat to these ecosystems that could significantly alter their vegetation structure and composition. Here, we examined drought tolerance in seedlings of seven common dry-forest tree species from the Indian subcontinent. We conducted a dry-down experiment on 3-wk-old seedlings, and asked whether the key plant functional traits, specific leaf area (SLA), leaf dry matter content (LDMC), seed size and stem specific density (SSD) were good predictors of seedling growth under well-watered conditions, and survival during drought. Seedlings displayed substantial drought tolerance with most seedlings surviving for more than 2 wk under protracted drought. Seed size in combination with SLA predicted seedling growth under well-watered conditions and seed size predicted survival under drought. In contrast to our expectations, seedlings with lower SSD survived for longer without water. Our results suggest that dry-forest species will be differentially affected by the predicted increases in the duration of growing-season droughts, and detrimental effects will be more severe for species with smaller seeds.

Type
Research Article
Copyright
© Cambridge University Press 2019 

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References

Literature cited

Allen, K, Dupuy, JM, Gei, MG, Hulshof, C, Medvigy, D, Pizano, C, Salgado-Negret, B, Smith, CM, Trierweiler, A, Van Bloem, SJ, Waring, BG, Xu, X and Powers, JS (2017) Will seasonally dry tropical forests be sensitive or resistant to future changes in rainfall regimes? Environmental Research Letters 12, 023001.CrossRefGoogle Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24, 127135.CrossRefGoogle ScholarPubMed
Caesar, A (2003) Synergistic interaction of soilborne plant pathogens and root-attacking insects in classical biological control of an exotic rangeland weed. Biological Control 28, 144153.CrossRefGoogle Scholar
Castro-Diez, P, Puyravaud, J, Cornelissen, J and Villar-Salvador, P (1998) Stem anatomy and relative growth rate in seedlings of a wide range of woody plant species and types. Oecologia 116, 5766.CrossRefGoogle ScholarPubMed
Cornelissen, JHC, Cerabolini, B, Castro-Diez, P, Villar-Salvador, P, Montserrat-Martí, G, Puyravaud, J, Maestro, M, Werger, MJA and Aerts, R (2003) Functional traits of woody plants: correspondence of species rankings between field adults and laboratory-grown seedlings? Journal of Vegetation Science 14, 311322.CrossRefGoogle Scholar
Cramer, MD, Van Cauter, A and Bond, WJ (2010) Growth of N2-fixing African savanna Acacia species is constrained by below-ground competition with grass. Journal of Ecology 98, 156167.CrossRefGoogle Scholar
Dalling, JW and Hubbell, S (2002) Seed size, growth rate and gap microsite conditions as determinants of recruitment success for pioneer species. Journal of Ecology 90, 557568.CrossRefGoogle Scholar
Davis, MA, Wrage, KJ and Reich, PB (1998) Competition between tree seedlings and herbaceous vegetation: support for a theory of resource supply and demand. Journal of Ecology 86, 652661.CrossRefGoogle Scholar
Dios, VR, Weltzin, JF, Sun, W, Huxman, TE and Williams, DG (2014) Transitions from grassland to savanna under drought through passive facilitation by grasses. Journal of Vegetation Science 25, 937946.CrossRefGoogle Scholar
Engelbrecht, BM and Kursar, TA (2003) Comparative drought-resistance of seedlings of 28 species of co-occurring tropical woody plants. Oecologia 136, 383393.CrossRefGoogle ScholarPubMed
Engelbrecht, BM, Dalling, JW, Pearson, TR, Wolf, RL, Galvez, DA, Koehler, T, Tyree, MT and Kursar, TA (2006) Short dry spells in the wet season increase mortality of tropical pioneer seedlings. Oecologia 148, 258269.CrossRefGoogle ScholarPubMed
Enquist, BJ, West, GB, Charnov, EL and Brown, JH (1999) Allometric scaling of production and life-history variation in vascular plants. Nature 401, 907911.CrossRefGoogle Scholar
Fenner, M (1983) Relationships between seed weight, ash content and seedling growth in twenty-four species of Compositae. New Phytologist 95, 697706.CrossRefGoogle Scholar
Grant, OM (2012) Understanding and exploiting the impact of drought stress on plant physiology. In Ahmad, P and Prasad, MNV (eds), Abiotic Stress Responses in Plants. New York: Springer, pp. 89104.CrossRefGoogle Scholar
Grossnickle, SC (2005) Importance of root growth in overcoming planting stress. New Forests 30, 273294.CrossRefGoogle Scholar
Grossnickle, SC (2012) Why seedlings survive: influence of plant attributes. New Forests 43, 711738.CrossRefGoogle Scholar
Hacke, UG, Sperry, JS, Pockman, WT, Davis, SD and McCulloh, KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126, 457461.CrossRefGoogle ScholarPubMed
Hossain, MA, Uddin, MS, Shumi, W and Ab Shukor, NA (2014) Depulping of fruits and soaking the seeds enhances the seed germination and initial growth performance of Terminalia belerica Roxb. seedlings. American Journal of Plant Sciences 5, 714.CrossRefGoogle Scholar
IPCC (2013) Climate Change 2013: The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, 1586 pp.Google Scholar
Jurado, E and Westoby, M (1992) Seedling growth in relation to seed size among species of arid Australia. Journal of Ecology 80, 407416.CrossRefGoogle Scholar
Khurana, E and Singh, J (2001) Ecology of seed and seedling growth for conservation and restoration of tropical dry forest: a review. Environmental Conservation 28, 3952.CrossRefGoogle Scholar
Khurana, E and Singh, J (2004) Germination and seedling growth of five tree species from tropical dry forest in relation to water stress: impact of seed size. Journal of Tropical Ecology 20, 385396.CrossRefGoogle Scholar
King, DA, Davies, SJ, Tan, S and Noor, NS (2006) The role of wood density and stem support costs in the growth and mortality of tropical trees. Journal of Ecology 94, 670680.CrossRefGoogle Scholar
Leishman, MR and Westoby, M (1994) The role of seed size in seedling establishment in dry soil conditions– experimental evidence from semi-arid species. Journal of Ecology 82, 249258.CrossRefGoogle Scholar
Leishman, MR, Wright, IJ, Moles, AT and Westoby, M (2000) The evolutionary ecology of seed size. In Fenner, M (ed.), Seeds: The Ecology of Regeneration in Plant Communities. 2nd Edn. Wallingford: CABI Publishing, pp. 3157.CrossRefGoogle Scholar
Lens, F, Tixier, A, Cochard, H, Sperry, JS, Jansen, S and Herbette, S (2013) Embolism resistance as a key mechanism to understand adaptive plant strategies. Current Opinion in Plant Biology 16, 287292.CrossRefGoogle ScholarPubMed
Lieberman, D and Li, M (1992) Seedling recruitment patterns in a tropical dry forest in Ghana. Journal of Vegetation Science 3, 375382.CrossRefGoogle Scholar
Markesteijn, L and Poorter, L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. Journal of Ecology 97, 311325.CrossRefGoogle Scholar
Martínez-Cabrera, HI, Jones, CS, Espino, S and Schenk, HJ (2009) Wood anatomy and wood density in shrubs: responses to varying aridity along transcontinental transects. American Journal of Botany 96, 13881398.CrossRefGoogle ScholarPubMed
Milberg, P and Lamont, BB (1997) Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient-poor soils. New Phytologist 137, 665672.CrossRefGoogle Scholar
Miles, L, Newton, AC, Defries, RS, Ravilious, C, May, I, Blyth, S, Kapos, V and Gordon, JE (2006) A global overview of the conservation status of tropical dry forests. Journal of Biogeography 33, 491505.CrossRefGoogle Scholar
Moles, AT and Westoby, M (2004a) Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 92, 372383.CrossRefGoogle Scholar
Moles, AT and Westoby, M (2004b) What do seedlings die from and what are the implications for evolution of seed size? Oikos 106, 193199.CrossRefGoogle Scholar
Munné-Bosch, S and Alegre, L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Functional Plant Biology 31, 203216.CrossRefGoogle Scholar
Padilla, FM, De Dios Miranda, J and Pugnaire, FI (2007) Early root growth plasticity in seedlings of three Mediterranean woody species. Plant and Soil 296, 103113.CrossRefGoogle Scholar
Pérez-Harguindeguy, N, Díaz, S, Garnier, E, Lavorel, S, Poorter, H, Jaureguiberry, P, Bret-Harte, M, Cornwell, W, Craine, J, Gurvich, D, Urcelay, C, Veneklaas, E, Reich, P, Poorter, L, Wright, I, Ray, P, Enrico, L, Pausas, J, De Vos, A, Buchmann, N, Funes, G, Quetier, F, Hodgson, J, Thompson, K, Morgan, H, Ter Steege, H, Van Der Heijden, M, Sack, L, Blonder, B, Poschlod, P, Vaieretti, M, Conti, G, Staver, A, Aquino, S and Cornellissen, H (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167234.CrossRefGoogle Scholar
Pineda-Garcia, F, Paz, H and Meinzer, FC (2013) Drought resistance in early and late secondary successional species from a tropical dry forest: the interplay between xylem resistance to embolism, sapwood water storage and leaf shedding. Plant, Cell & Environment 36, 405418.CrossRefGoogle ScholarPubMed
Poorter, L and Markesteijn, L (2008) Seedling traits determine drought tolerance of tropical tree species. Biotropica 40, 321331.CrossRefGoogle Scholar
Pyke, DA and Thompson, JN (1986) Statistical analysis of survival and removal rate experiments. Ecology 67, 240245.CrossRefGoogle Scholar
Reich, PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275301.CrossRefGoogle Scholar
Reich, PB, Ellsworth, D and Walters, M (1998) Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12, 948958.CrossRefGoogle Scholar
Ritz, C, Baty, F, Streibig, JC and Gerhard, D (2015) Dose-response analysis using R. PloS ONE 10, e0146021.CrossRefGoogle ScholarPubMed
Schielzeth, H (2010) Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution 1, 103113.CrossRefGoogle Scholar
Seidel, H and Menzel, A (2016) Above-ground dimensions and acclimation explain variation in drought mortality of Scots pine seedlings from various provenances. Frontiers in Plant Science 7, 1014.CrossRefGoogle ScholarPubMed
Shipley, B (2006) Net assimilation rate, specific leaf area and leaf mass ratio: which is most closely correlated with relative growth rate? A meta-analysis. Functional Ecology 20, 565574.CrossRefGoogle Scholar
Shipley, B and Peters, R (1990) The allometry of seed weight and seedling relative growth rate. Functional Ecology 4, 523529.CrossRefGoogle Scholar
Singh, L and Singh, J (1991) Species structure, dry matter dynamics and carbon flux of a dry tropical forest in India. Annals of Botany 68, 263273.CrossRefGoogle Scholar
Slot, M and Poorter, L (2007) Diversity of tropical tree seedling responses to drought. Biotropica 39, 683690.CrossRefGoogle Scholar
Tyree, MT, Engelbrecht, BM, Vargas, G and Kursar, TA (2003) Desiccation tolerance of five tropical seedlings in Panama: relationship to a field assessment of drought performance. Plant Physiology 132, 14391447.CrossRefGoogle ScholarPubMed
Varma, V and Osuri, AM (2013) Black Spot: a platform for automated and rapid estimation of leaf area from scanned images. Plant Ecology 214, 15291534.CrossRefGoogle Scholar
Vertessy, R, Benyon, R, O’Sullivan, S and Gribben, P (1994) Leaf area and tree water use in a 15-year-old mountain ash forest, Central Highlands, Victoria. Cooperative Research Centre for Catchment Hydrology Technical Report 93.Google Scholar
Wolfe, BT (2017) Retention of stored water enables tropical tree saplings to survive extreme drought conditions. Tree Physiology 37, 469480.CrossRefGoogle ScholarPubMed
Wright, IJ and Westoby, M (2001) Understanding seedling growth relationships through specific leaf area and leaf nitrogen concentration: generalisations across growth forms and growth irradiance. Oecologia 127, 2129.CrossRefGoogle ScholarPubMed
Wright, IJ, Falster, DS, Pickup, M and Westoby, M (2006) Cross-species patterns in the coordination between leaf and stem traits, and their implications for plant hydraulics. Physiologia Plantarum 127, 445456.CrossRefGoogle Scholar
Wright, IJ, Reich, PB, Westoby, M, Ackerly, DD, Baruch, Z, Bongers, F, Cavender-Bares, J, Chapin, T, Cornelissen, JH, Diemer, M, Flexas, J, Garnier, E, Groom, PK, Gulias, J, Hikosaka, K, Lamont, BB, Lee, T, Lee, W, Lusk, C, Midgley, JJ, Navas, ML, Niinemets, U, Oleksyn, J, Osada, N, Poorter, H, Poot, P, Prior, L, Pyankov, VI, Roumet, C, Thomas, SC, Tjoelker, MG, Veneklaas, EJ and Villar, R (2004) The worldwide leaf economics spectrum. Nature 428, 821827.CrossRefGoogle ScholarPubMed
Wright, SJ, Kitajima, K, Kraft, NJB, Reich, PB, Wright, IJ, Bunker, DE, Condit, R, Dalling, JW, Davies, SJ, Díaz, S, Engelbrecht, BMJ, Harms, KE, Hubbell, SP, Marks, CO, Ruiz-Jaen, MC, Salvador, CM and Zanne, AE (2010) Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91, 36643674.CrossRefGoogle ScholarPubMed