Abstract
Species in dry environments may adjust their anatomical and physiological behaviors by adopting safer or more efficient strategies. Thus, species distributed across a water availability gradient may possess different phenotypes depending on the specific environmental conditions to which they are subjected. Leaf and vascular tissues are plastic and may vary strongly in response to environmental changes affecting an individual’s survival and species distribution. To identify whether and how legumes leaves vary across a water availability gradient in a seasonally dry tropical forest, we quantified leaf construction costs and performed an anatomical study on the leaves of seven legume species. We evaluated seven species, which were divided into three categories of rainfall preference: wet species, which are more abundant in wetter areas; indifferent species, which are more abundant and occur indistinctly under both rainfall conditions; and dry species, which are more abundant in dryer areas. We observed two different patterns based on rainfall preference categories. Contrary to our expectations, wet and indifferent species changed traits in the sense of security when occupying lower rainfall areas, whereas dry species changed some traits when more water was available, such as increasing cuticle and spongy parenchyma thickness, or producing smaller and more numerous stomata. Trischidium molle, the most plastic and wet species, exhibited a similar strategy to the dry species. Our results corroborate the risks to vegetation under future climate change scenarios as stressed species and populations may not endure even more severe conditions.
Similar content being viewed by others
Data availability
We declare that the data presented in the article “Drought-adapted leaves are produced even when more water is available in dry tropical forests” may be available upon request to the authors.
References
Anderegg WRL, Flint A, Huang CY et al (2015a) Tree mortality predicted from drought-induced vascular damage. Nat Geosci 8:367–371. https://doi.org/10.1038/ngeo2400
Anderegg WRL, Schwalm C, Biondi F et al (2015b) Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 80(349):528–532. https://doi.org/10.1126/science.aab1833
Bento JPSP, Scremin-Dias E, Alves FM et al (2020) Phylogenetic implications of the anatomical study of the Amburaneae clade (Fabaceae: Faboideae). Bot J Linn Soc. https://doi.org/10.1093/botlinnean/boaa019
Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00225
Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379. https://doi.org/10.1016/S0168-9452(02)00135-8
Brodribb TJ, Mcadam SA, Carins Murphy MR (2017) Xylem and stomata, coordinated through time and space. Plant Cell Environ 40:872–880. https://doi.org/10.1111/pce.12817
Bucci SJ, Goldstein G, Meinzer FC et al (2004) Functional convergence in hydraulic architecture and water relations of tropical savanna trees: from leaf to whole plant. Tree Physiol 24:891–899. https://doi.org/10.1093/treephys/24.8.891
Buckley TN, Sack L, Gilbert ME (2011) The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiol 156:962–973. https://doi.org/10.1104/pp.111.175638
Buckley TN, Sack L, Farquhar GD (2017) Optimal plant water economy. Plant Cell Environ 40:881–896. https://doi.org/10.1111/pce.12823
Camarero JJ, Gazol A, Sangüesa-Barreda G et al (2018) Forest growth responses to drought at short- and long-term scales in Spain: squeezing the stress memory from tree rings. Front Ecol Evol 6:1–11. https://doi.org/10.3389/fevo.2018.00009
Carmona CP, de Bello F, Mason NWH, Lepš J (2016) Traits without borders: integrating functional diversity across scales. Trends Ecol Evol 31:382–394. https://doi.org/10.1016/j.tree.2016.02.003
Cosme LHM, Schietti J, Costa FRC, Oliveira RS (2017) The importance of hydraulic architecture to the distribution patterns of trees in a central Amazonian forest. New Phytol. https://doi.org/10.1111/nph.14508
da Silva JMC, Barbosa LCF (2017) Impact of human activities on the Caatinga. In: da Silva JMC, Leal IR, Tabarelli M (eds) Caatinga, 1st edn. Springer International Publishing, Cham, pp 359–368
da Silva PF, de Lima JRS, Antonino ACD et al (2017) Seasonal patterns of carbon dioxide, water and energy fluxes over the Caatinga and grassland in the semi-arid region of Brazil. J Arid Environ. https://doi.org/10.1016/j.jaridenv.2017.09.003
Dayer S, Herrera JC, Dai Z et al (2020) The sequence and thresholds of leaf hydraulic traits underlying grapevine varietal differences in drought tolerance. J Exp Bot 71:4333–4344. https://doi.org/10.1093/jxb/eraa186
de Souza Cavalcanti LC, de Barros Corrêa AC (2014) Pluviosidade no parque nacional do Catimbau (Pernambuco): seus condicionantes e seus efeitos sobre a paisagem. Geografia 23:133–156
de Lima ALA, de Sá Barretto Sampaio EV, de Castro CC et al (2012) Do the phenology and functional stem attributes of woody species allow for the identification of functional groups in the semiarid region of Brazil? Trees Struct Funct 26:1605–1616. https://doi.org/10.1007/s00468-012-0735-2
De Wispelaere L, Bodé S, Hervé-Fernández P et al (2017) Plant water resource partitioning and isotopic fractionation during transpiration in a seasonally dry tropical climate. Biogeosciences 14:73–88. https://doi.org/10.5194/bg-14-73-2017
Domec J-C, Smith DD, McCulloh KA (2016) A synthesis of the effects of atmospheric carbon dioxide enrichment on plant hydraulics: implications for whole-plant water use efficiency and resistance to drought. Plant Cell Environ. https://doi.org/10.1111/pce.12843
Engelbrecht BMJJ, Comita LS, Condit R et al (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82. https://doi.org/10.1038/nature05747
Falcão HM, Medeiros CD, Silva BLR et al (2015) Phenotypic plasticity and ecophysiological strategies in a tropical dry forest chronosequence: a study case with Poincianella pyramidalis. For Ecol Manag 340:62–69. https://doi.org/10.1016/j.foreco.2014.12.029
Falcão HM, Medeiros CD, Almeida-Cortez J, Santos MG (2017) Leaf construction cost is related to water availability in three species of different growth forms in a Brazilian tropical dry forest. Theor Exp Plant Physiol 29:95–108. https://doi.org/10.1007/s40626-017-0087-9
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1 km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315
Figueiredo KV, Oliveira MT, Arruda ECP et al (2015) Changes in leaf epicuticular wax, gas exchange and biochemistry metabolism between Jatropha mollissima and Jatropha curcas under semi-arid conditions. Acta Physiol Plant. https://doi.org/10.1007/s11738-015-1855-2
Fleta-Soriano E, Munné-Bosch S (2016) Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci 7:1–6. https://doi.org/10.3389/fpls.2016.00143
Franklin GL (1945) Preparation of thin sections of synthetic resins and wood-resin composites, and a new macerating method for wood. Nature 155:51–51. https://doi.org/10.1038/155051a0
Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4:97–115
Hacke UG, Spicer R, Schreiber SG, Plavcov L (2016) An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Environ. https://doi.org/10.1111/pce.12777
IBGE (2002) Mapa de Solos Brasileiros—IBGE.pdf
Johansen DA (1940) Plant microtechnique. New York
Kevekordes KG, McCully ME, Canny MJ (1988) The occurrence of an extended bundle sheath system (paraveinal mesophyll) in the legumes. Can J Bot 66:94–100. https://doi.org/10.1139/b88-014
Kiorapostolou N, Petit G (2019) Similarities and differences in the balances between leaf, xylem and phloem structures in Fraxinus ornus along an environmental gradient. Tree Physiol 39:234–242. https://doi.org/10.1093/treephys/tpy095
Kiorapostolou N, Camarero JJ, Carrer M et al (2020) Scots pine trees react to drought by increasing xylem and phloem conductivities. Tree Physiol 40:774–781. https://doi.org/10.1093/treephys/tpaa033
Kottek M, Grieser J, Beck C et al (2006) World map of Köppen − Geiger climate classification. Meteorol Z 15:259–263. https://doi.org/10.1127/0941-2948/2006/0130
Kraus JE, De Sousa HC, Rezende MH et al (1998) Astra blue and basic fuchsin double staining of plant materials. Biotech Histochem 73:235–243. https://doi.org/10.3109/10520299809141117
Li X, Liu F (2016) Drought stress memory and drought stress tolerance in plants: biochemical and molecular basis. Drought stress tolerance in plants, vol 1. Springer International Publishing, Cham, pp 17–44
Li L, McCormack ML, Ma C et al (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18:899–906. https://doi.org/10.1111/ele.12466
Maiti R, Rodríguez HG, Balboa PCR et al (2016) Leaf surface anatomy in some woody plants from northeastern Mexico. Pak J Bot 48:1825–1831
Marinho CR, Oliveira RB, Teixeira SP (2016) The uncommon cavitated secretory trichomes in Bauhinia s.s. (Fabaceae): the same roles in different organs. Bot J Linn Soc 180:104–122. https://doi.org/10.1111/boj.12354
McClendon JH (1992) Photographic survey of the occurrence of bundle-sheath extensions in deciduous dicots. Plant Physiol 99:1677–1679. https://doi.org/10.1104/pp.99.4.1677
Medeiros CD, Falcão HM, Almeida-Cortez J et al (2017) Leaf epicuticular wax content changes under different rainfall regimes, and its removal affects the leaf chlorophyll content and gas exchanges of Aspidosperma pyrifolium in a seasonally dry tropical forest. South Afr J Bot 111:267–274. https://doi.org/10.1016/J.SAJB.2017.03.033
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) Vegan: community ecology package. R package version 2.6-2. https://CRAN.R-project.org/package=vegan
PBMC (2014) Avaliação de modelos globais e regionais climáticos. In: Base científica das mudanças climáticas. pp 278–319
Penning de Vries FWT, Brunsting AHM, Van Laar HH (1974) Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol 45:339–377. https://doi.org/10.1016/0022-5193(74)90119-2
Pereira S, Figueiredo-Lima K, Oliveira AFM, Santos MG (2019) Changes in foliar epicuticular wax and photosynthesis metabolism in evergreen woody species under different soil water availability. Photosynthetica. https://doi.org/10.32615/ps.2019.013
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rasband W (2018) ImageJ. US National Institutes of Health, Bethesda, Mar
Rito KF, Arroyo-Rodríguez V, Queiroz RT et al (2017) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. J Ecol 105:828–838. https://doi.org/10.1111/1365-2745.12712
Rivas R, Santos MG (2023) The desert plant Calotropis procera maintains C3 photosynthetic metabolism under salt stress. Theor Exp Plant Physiol 35:1–16. https://doi.org/10.1007/s40626-022-00265-x
Rodrigues TM, Esteves Amaro AC, Fernandes Boaro CS et al (2017) Four distinct leaf types in the Brazilian cerrado, based on bundle sheath extension morphology. Botany 95:1171–1178. https://doi.org/10.1139/cjb-2017-0073
Rodrigues-Filho S, Junior DSR, Martins E, et al (2016) Implicações Para a Sustentabilidade Regional No Brasil
Roeser K (1972) Die Nadel der Schwarzkiefer—Massenprodukt und Kunstwerk der Natur. Mikrokosmos 61:33–36
Roth I (1990) Peculiar surface structures of tropical leaves for gas exchange, guttation, and light capture. https://doi.org/10.1007/978-94-009-1872-6_3
Rutten T, Krüger C, Melzer M et al (2003) Discovery of an extended bundle sheath in Ricinus communis L. and its role as a temporal storage compartment for the iron chelator nicotianamine. Planta 217:400–406. https://doi.org/10.1007/s00425-003-1010-y
Salisbury EJ (1928) I. On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philos Trans R Soc London Ser B, Contain Pap a Biol Character 216:1–65. https://doi.org/10.1098/rstb.1928.0001
Santos MG, Oliveira MT, Figueiredo KV et al (2014) Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes? Theor Exp Plant Physiol 26:83–99. https://doi.org/10.1007/s40626-014-0008-0
Sevanto S (2014) Phloem transport and drought. J Exp Bot 65:1751–1759. https://doi.org/10.1093/jxb/ert467
Silva AC, Souza AF (2018) Aridity drives plant biogeographical sub regions in the Caatinga, the largest tropical dry forest and woodland block in South America. PLoS ONE 13:e0196130. https://doi.org/10.1371/journal.pone.0196130
Speckmann GJ, Post J, Dijkstra H (1965) The length of stomata as an indicator for polyploidy in rye-grasses. Euphytica 14:225–230. https://doi.org/10.1007/BF00149503
Sperry JS, Venturas MD, Anderegg WRL et al (2016) Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant Cell Environ. https://doi.org/10.1111/pce.12852
Tomás M, Flexas J, Copolovici L et al (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. J Exp Bot 64:2269–2281. https://doi.org/10.1093/jxb/ert086
Tombesi S, Frioni T, Poni S, Palliotti A (2018) Effect of water stress “memory” on plant behavior during subsequent drought stress. Environ Exp Bot 150:106–114. https://doi.org/10.1016/j.envexpbot.2018.03.009
Torres RR, Lapola DM, Gamarra NLR (2017) Future climate change in the Caatinga. In: da Silva JMC, Leal IR, Tabarelli M (eds) Caatinga. Springer International Publishing, Cham, pp 383–410
Villar R, Merino J (2001) Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol 151:213–226. https://doi.org/10.1046/j.1469-8137.2001.00147.x
Weston GD, Cass DD (1973) Observations on the development of the paraveinal mesophyll of soybean leaves. Bot Gaz 134:232–235. https://doi.org/10.1086/336708
Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734. https://doi.org/10.1111/1365-3040.ep11604754
Wylie RB (1952) The bundle sheath extension on leaves of dicotyledons. Am J Bot 39:645–651. https://doi.org/10.1086/336403
Yin H, Tariq A, Zhang B et al (2021) Coupling relationship of leaf economic and hydraulic traits of Alhagisparsifolia Shap in a hyper-arid desert ecosystem. Plants 10:1867. https://doi.org/10.3390/plants10091867
Zsögön A, Alves Negrini AC, Peres LEP et al (2015) A mutation that eliminates bundle sheath extensions reduces leaf hydraulic conductance, stomatal conductance and assimilation rates in tomato (Solanum lycopersicum). New Phytol 205:618–626. https://doi.org/10.1111/nph.13084
Acknowledgements
The authors thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (funding code—001). M. Santos are grateful to CNPq for the productivity grants. We are grateful to LAVe-UFMS to support our laboratory work. We would like to thank Mariana Santos, Lays Lins, and Sílvia Pereira for help with sampling, and Augusto Ribas with the statistical analyses.
Funding
This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/PELD 403770/2012-2), (CNPq/Universal 428161/2018-9) and T. Yule scholarship.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Tamires Soares Yule, Mauro Guida dos Santos and Rosani do Carmo de Oliveira Arruda. The first draft of the manuscript was written by Tamires Soares Yule and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
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 (e.g. a society or other partner) 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
Yule, T.S., de Oliveira Arruda, R.d.C. & Santos, M.G. Drought-adapted leaves are produced even when more water is available in dry tropical forest. J Plant Res 137, 49–64 (2024). https://doi.org/10.1007/s10265-023-01505-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-023-01505-0