Seasonal variations of leaf traits and drought adaptation strategies of four common woody species in South Texas, USA

Abstract

Understanding physiological responses and drought adaptation strategies of woody plant leaf traits in sub-humid to semi-arid regions is of vital importance to understand the interplay between ecological processes and plant resource-allocation strategies of different tree species. Seasonal variations of leaf morphological traits, stoichiometric traits and their relationships of two drought tolerant woody species, live oak (Quercus virginiana) and honey mesquite (Prosopis glandulosa) and two less drought tolerant species, sugarberry (Celtis laevigata) and white ash (Fraxinus americana) were analyzed in a sub-humid to semi-arid area of south Texas, USA. Our findings demonstrate that for the two drought tolerant species, the leguminous P. glandulosa had the highest specific leaf area, leaf N, P, and lowest leaf area and dry mass, indicating that P. glandulosa adapts to an arid habitat by decreasing leaf area, thus reducing water loss, reflecting a resource acquisition strategy. While the evergreen species Q. virginiana exhibited higher leaf dry mass, leaf dry matter content, C content, C:N, C:P and N:P ratios, adapts to an arid habitat through increased leaf thickness and thus reduced water loss, reflecting a resource conservation strategy in south Texas. For the two less drought tolerant deciduous species, the variations of leaf traits in C. laevigata and F. americana varied between Q. virginiana and P. glandulosa, reflecting a trade-off between rapid plant growth and nutrient maintenance in a semi-arid environment.

Keywords

Drought adaptation strategies / Leaf traits / Seasonal variations / South Texas / Woody species

References

Ågren GI. Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol Evol Syst, 2008, 39: 153-170.

Ali AM, Darvishzadeh R, Skidmore AK, Duren IV, Heiden U, Heurich M. Estimating leaf functional traits by inversion of PROSPECT: assessing leaf dry matter content and specific leaf area in mixed mountainous forest. Int J Appl Earth Obs, 2016, 45: 66-76.

Ansley RJ, Jacoby PW, Cuomo GJ. Water relations of honey mesquite following severing of lateral roots: influence of location of subsurface water. J Range Manag, 1990, 43: 436-442.

Boege K. Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia, 2005, 143: 117-125.

Burak S, Hamdi GK, Abdullah Ç, Hakan Y. Comparison of leaf traits (SLA and LMA) on different populations of Alcea apterocarpa. J Biol Chem, 2016, 44: 125-131.

Casper BB, Forseth IN, Kempenich H, Seltzer S, Xavier K. Drought prolongs leaf life span in the herbaceous desert perennial Cryptantha flava. Funct Ecol, 2001, 15: 740-747.

Cernusak LA, Winter K, Turner BL. Leaf nitrogen to phosphorus ratios of tropical trees: experimental assessment of physiological and environmental controls. New Phytol, 2010, 185: 770-779.

Chandra A, Pathak PS, Bhatt RK, Dubey A. Variation in drought tolerance of different Stylosanthes accessions. Biol Plant, 2004, 48: 457-460.

Comstock J, Mencuccini M. Control of stomatal conductance by leaf water potential in Hymenoclea salsola, a desert subshrub. Plant Cell Environ, 1998, 21: 1029-1038.

Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot, 2003, 51: 335-380.

Cornelissen JHC, Quested HM, Logtestijn RSP, Perez-Harguindeguy N, Gwynn-Jones D, Diaz S, Callaghan TV, Press MC, Aerts R. Foliar pH as a new plant trait: can it explain variation in foliar chemistry and carbon cycling processes among subarctic plant species and types?. Oecologia, 2006, 147: 315-326.

Costa-Saura JM, Martínez-Vilalta J, Trabucco A, Spano D, Mereu S. Specific leaf area and hydraulic traits explain niche segregation along an aridity gradient in Mediterranean woody species. Perspect Plant Ecol, 2016, 21: 23-30.

Craine JM, Frochle J, Tilman DG, Wedin DA, Chapin FS. The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos, 2001, 93: 274-285.

Cunningham AB. Applied ethnobotany: people, wild plant use and conservation, 2001, Sterling: Earthscan Publications Ltd.

Diaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR. The plant traits that drive ecosystems: evidence from three continents. J Veg Sci, 2004, 15: 295-304.

Eamus D, Prior L. Ecophysiology of trees of seasonally dry tropics: comparisons among phenologies. Adv Ecol Res, 2001, 32: 113-197.

Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW. Nutritional constraints in terrestrial and freshwater food webs. Nature, 2000, 408: 578-580.

Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol, 2010, 186: 593-608.

Franco AC, Bustamante MMC, Caldas LS, Coradin Vera TR. Leaf functional traits of Neotropical savanna trees in relation to seasonal water deficit. Trees, 2005, 19: 326-335.

Garrish V, Cernusak LA, Winter K, Turner BL. Nitrogen to phosphorus ratio of plant biomass versus soil solution in a tropical pioneer tree, Ficus insipida. J Exp Bot, 2010, 61: 3735-3748.

Golubov J, Mandujano MC, Eguiarte LE. The paradox of mesquites (Prosopis spp.): invading species of biodiversity enhancers. Bol Soc Bot Mex, 2001, 69: 21-28.

Güsewell S. N:P ratios in terrestrial plants: variation and functional significance. New Phytol, 2004, 164: 243-266.

Han WX, Fang JY, Guo DL, Zhang Y. Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol, 2005, 168: 377-385.

Harms W. Burns R, Honkala BH. Quercus virginiana. Silvics of North America: 1. Conifers; 2. hardwoods. Agriculture handbook, 1990, Washington: USDA Forest Service.

Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF. Plant allometry, stoichiometry and the temperature-dependence of primary productivity. Glob Ecol Biogeogr, 2005, 14: 585-598.

Koerselman W, Meuleman AFM. The vegetation N/P ratio—a new tool to detect the nature of nutrient limitation. J Appl Ecol, 1996, 33: 1441-1450.

Kuo S. Sparks DI, Page AI, Helmke PA, Leoppert RH, Soltanpour PN, Tabatabbi MA, John CT, Summer ME. Phosphorus. Chemical methods of soil analysis. Part 3, soil science society of America, 1996, Madison: American Society of Agronomy 869 919

Kursar TA, Coley PD. Convergence in defense syndromes of young leaves in tropical rainforests. Biochem Syst Ecol, 2003, 31: 929-949.

Lambers H, Poorter H. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res, 1992, 23: 187-261.

Laureano RG, Lazo YO, Linares JC, Luque A, Martínez F, Seco JI, Merino J. The cost of stress resistance: construction and maintenance costs of leaves and roots in two populations of Quercus ilex. Tree Physiol, 2008, 28: 1721-1728.

Lavorel S, Díaz S, Cornelissen JHC, Garnier E, Harrison SP, McIntyre S, Pausas JG, Perez-Harguindeguy N, Roumet C, Urcelay C. Canadell JG, Pataki DE, Pitelka LF. Plant functional types: are we getting any closer to the Holy Grail?. Terrestrial ecosystems in a changing World, 2007, Berlin: Springer 149 164

Li JY, Guo QX, Zhang JX, Korpelainen H, Li CY. Effects of nitrogen and phosphorus supply on growth and physiological traits of two Larix species. Environ Exp Bot, 2016, 130: 206-215.

Marron N, Dreyer E, Boudouresque E, Delay D, Petit JM, Delmotte FM, Brignolas F. Impact of successive drought and re-watering cycles on growth and specific leaf area of two Populus canadensis (Moench) clones, “Dorskamp” and “Luisa_Avanzo”. Tree Physiol, 2003, 23: 1225-1235.

Marschner H, Marschner P. Marschner’s mineral nutrition of higher plants, 2012, London: Academic press.

Mediavilla S, Garcia-ciudad A, Garcia-ciudad B, Escudero A. Testing the correlations between leaf life span and leaf structural reinforcement in 13 species of European mediterranean woody plants. Funct Ecol, 2008, 22: 787-793.

Niinemets Ü. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 2001, 82: 453-469.

Niklas KJ, Cobb ED, Niineemets Ü, Reich PB, Sellin A, Shipley B, Wright IJ. “Diminishing returns” in the scaling of functional leaf traits across and within species groups. PNAS, 2007, 104: 8891-8896.

Pierce LL, Running SW, Walker J. Regional-scale relationships of leaf-area index to specific leaf-area and leaf nitrogen-content. Ecol Appl, 1994, 4: 313-321.

Poorter H, De Jong RA. Comparison of specific leaf area chemical composition and leaf construction costs of field plants from 15 habitats differing in productivity. New Phytol, 1999, 143: 163-176.

Poorter H, Garnier E. Pugnaire FI, Valladares F. Ecological significance of inherent variation in relative growth rate and its components. Functional plant ecology, 2007 2 Boca Raton: CRC Press 67 100

Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol, 2009, 182: 565-588.

Pringle EG, Adams RI, Broadbent E, Busby PE, Donatti CI, Kurten EL. Distinct leaf-trait syndromes of evergreen and deciduous trees in a seasonally dry tropical forest. Biotropica, 2011, 43: 299-308.

Prior LD, Eamus D, Bowman DMJS. Leaf attributes in the seasonally dry tropics: a comparison of four habitats in northern Australia. Funct Ecol, 2003, 17: 504-515.

Qin J, Xi WM, Rahmlow A, Kong HY, Zhang Z, Shangguan ZP. Effects of forest plantation types on leaf traits of Ulmus pumila and Robinia pseudoacacia on the Loess Plateau, China. Ecol Eng, 2016, 97: 416-425.

Reich PB, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS, 2004, 101: 11001-11006.

Reich PB, Walters MB, Ellsworth DS. Leaf life-span in relation to leaf, plant and stand characteristics among diverse ecosystems. Ecol Monogr, 1992, 62: 365-392.

Reich PB, Walters MB, Ellsworth DS. From tropics to tundra: global convergence in plant functioning. PNAS, 1997, 94: 13730-13734.

Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD. Generality of leaf trait relationships: a test across six biomes. Ecology, 1999, 80: 1955-1969.

Reich PB, Wright IJ, Cavender-Bares JM, Graine JM, Oleksyn J, Westoby M, Walters MB. The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci, 2003, 164: 143-164.

Reich PB, Wright IJ, Lusk CH. Predicting leaf physiology from simple plant and climate attributes: a global GLOPNET analysis. Ecol Appl, 2007, 17: 1982-1988.

Sardans J, Penuelas J, Roda F. Plasticity of leaf morphological traits, leaf nutrient content, and water capture in the Mediterranean evergreen oak Quercus ilex subsp. ballota in response to fertilization and changes in competitive conditions. Ecosicence, 2006, 13: 258-270.

Schmandt J, North GR, Clarkson J. The impact of global warming on texas, 2012 2 Austin: University of Texas Press.

Shipley B, Vile D, Garnier E, Wright I, Poorter H. Functional linkages between leaf traits and net photosynthetic rate: reconciling empirical and mechanistic models. Funct Ecol, 2005, 19: 602-615.

Silva JO, Espírito-Santo MM, Melo GA. Herbivory on Handroanthus ochraceus (Bignoniaceae) along a successional gradient in a tropical dry forest. Arthropod Plant Interact, 2012, 6: 45-57.

Silva JO, Espírito-Santoa MM, Moraisb HC. Leaf traits and herbivory on deciduous and evergreen trees in a tropical dry forest. Basic Appl Ecol, 2015, 16: 210-219.

Sterner RW, Elser JJ. Ecological stoichiometry: the biology of elements from molecules to the biosphere, 2002, Princeton: Princeton University Press.

Suter M, Edwards PJ. Convergent succession of plant communities is linked to species’ functional traits. Perspect Plant Ecol, 2013, 15: 217-225.

Tomlinson KW, Poorter L, Sterck FJ, Borghetti F, Ward D, de Bie S. Leaf adaptations of evergreen and deciduous trees of semi-arid and humid savannas on three continents. J Ecol, 2013, 101: 430-440.

Turner IM. Sclerophylly: primarily protective?. Funct Ecol, 1994, 8: 669-675.

Villar R, Merino JA. Comparison of leaf construction cost in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol, 2001, 151: 213-226.

Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E. Let the concept of trait be functional!. Oikos, 2007, 116: 882-892.

Wang LL, Zhao GX, Li M, Zhang MT, Zhang LF, Zhang XF, An LZJ, Xu S. C:N: P stoichiometry and leaf traits of halophytes in an arid saline environment, Northwest China. PLoS ONE, 2015, 10(3): 1-16.

Waring EF, Schwilk DW. Plant dieback under exceptional drought driven by elevation, not by plant traits, in Big Bend National Park, Texas, USA. Peer J, 2014, 2: 477.

Williams J, Gardener CJ. Stace HM, Edye LA. Environmental constraints to growth and survival of Stylosanthes. The biology and agronomy of stylosanthes, 1984, Sydney: Academic Press 181 201

Wilson PJ, Thompson KEN, Hodgson JG. Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytol, 1999, 143: 155-162.

Wright IJ, Westoby M. Understanding seedling growth relationships through specific leaf area and leaf nitrogen concentration: generalizations across growth forms and growth irradiance. Oecologia, 2001, 127: 21-29.

Wright IJ, Reich PB, Westoby M, Acherly DD, Baruch Z, Bongers F, Cavender-Bares J, Johannes HC, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley J, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R. The worldwide leaf economics spectrum. Nature, 2004, 428: 821-827.

Wright IJ, Reich PB, Cornelissen JHC, Falstar DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M. Assessing the generality of global leaf trait relationships. New Phytol, 2005, 166: 485-496.

Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M. Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr, 2005, 14: 411-421.

Yang X, Tang JW, Mustard JF, Wu J, Zhao KG, Serbin S, Lee JE. Seasonal variability of multiple leaf traits captured by leaf spectroscopy at two temperate deciduous forests. Remote Sens Environ, 2016, 179: 1-12.

Zhao N, He N, Wang Q, Zhang X, Wang R, Xu Z. The altitudinal patterns of leaf C:N: P stoichiometry are regulated by plant growth form, climate and soil on Changbai Mountain, China. PLoS ONE, 2014, 9: 95-96.