Mesophyll thickness and sclerophylly among Calotropis procera morphotypes reveal water-saved adaptation to environments

  • Marcelo F. PompelliEmail author
  • Keila R. Mendes
  • Marcio V. Ramos
  • José N. B. Santos
  • Diaa T. A. Youssef
  • Jaqueline D. Pereira
  • Laurício Endres
  • Alfredo Jarma-Orozco
  • Rodolfo Solano-Gomes
  • Betty Jarma-Arroyo
  • André L. J. Silva
  • Marcos A. Santos
  • Werner C. Antunes


Calotropis procera (Aiton) Dryand (Apocynaceae) is a native species in tropical and subtropical Africa and Asia. However, due to its fast growing and drought-tolerant, it has become an invasive species when it was introduced into Central and South America, as well as the Caribbean Islands. Currently, C. procera displays a wide distribution in the world. Invasiveness is important, in particular, because many invasive species exert a high reproductive pressure on the invaded communities or are highly productive in their new distributed areas. It has been suggested that a very deep root system and a high capacity to reduce stomatal conductance during water shortage could allow this species to maintain the water status required for a normal function. However, the true mechanism behind the successful distribution of C. procera across wet and dry environments is still unknown. C. procera leaves were collected from 12 natural populations in Brazil, Colombia and Mexico, ranging from wet to dry environments during 2014–2015. Many traits of morphology and anatomy from these distinct morphotypes were evaluated. We found that C. procera leaves had a considerable capacity to adjust their morphological, anatomical and physiological traits to different environments. The magnitude of acclimation responses, i.e., plasticity, had been hypothesized to reflect the specialized adaptation of plant species to a particular environment. However, allometric models for leaf area (LA) estimation cannot be grouped as a single model. Leaves are narrower and thicker with low amounts of air spaces inside the leaf parenchyma in wet environments, while they are broader and thinner with a small number of palisade cell layers in dry environments. Based on these, we argue that broader and thinner leaves of C. procera dissipate incident energy at the expense of a higher rate of transpiration to survive in environments in which water is the most limiting factor and to compete in favorable wet environments.


invasive plant energy budget leaf anatomy morphological trait specific leaf area 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



The research were funded by the National Council for Scientific and Technological Development (CNPq; 470476/2011-7), the Foundation for Science and Technology of Pernambuco, Brazil (APQ-0077-5.01/09, DCR-0034-2.03/13) and the scholarship granted to the first author. The authors would also like to thank Dr. Jarcilene S ALMEIDA-CORTEZ (Department of Botany, Federal University of Pernambuco, Brazil) for his help with the field collections and Dr. Carlos A SCAPIM (Department of Agronomy, Maringá State University, Brazil) for his assistance on heritability. In addition, the authors extend special thanks to Dr. Hendrik POORTER (Forschungszentrum Jülich GmbH, Plant Sciences, Jülich, Germany) and Dr. Sidnei M THOMAZ (Department of Biology, Maringá State University, Brazil) for their kind revisions of this manuscript.


  1. Alberio C, Comparatore V. 2014. Patterns of woody plant invasion in an Argentinean coastal grassland. Acta Oecologia, 54(1): 65–71.CrossRefGoogle Scholar
  2. Antunes W C, Pompelli M F, Carretero D M, et al. 2008. Allometric models for non-destructive leaf area estimation in coffee (Coffea arabica and Coffea canephora). Annals of Applied Biology, 153(1): 33–40.CrossRefGoogle Scholar
  3. Antunes W C, Daloso D M, Pinheiro D P, et al. 2017. Guard cell-specific down-regulation of the sucrose transporter SUT1 leads to improved water use efficiency and reveals the interplay between carbohydrate metabolism and K+ accumulation in the regulation of stomatal opening. Environmental Experimental Botany, 135(1): 73–85.CrossRefGoogle Scholar
  4. Arterburn M A, Jones S S, Kidwell K K. 2010. Plant breeding and genetics. In: Verheye W H. Soils, Plant Growth and Crop Production. United Kingdon: EOLSS Publishers, 184–211.Google Scholar
  5. Bacelar E A, Moutinho-Pereira J M, Gonçalves B C, et al. 2007. Changes in growth, gas exchange, xylem hydraulic properties and water use efficiency of three olive cultivars under contrasting water availability regimes. Environmental Experimental Botany, 60(2): 183–192.CrossRefGoogle Scholar
  6. Bjorksten T A, Fowler K, Pomiankowski A. 2000. What does sexual trait FA tell us about stress? Trends in Ecology and Evolution, 15(4): 163–166.CrossRefGoogle Scholar
  7. Blossey B, Nötzold R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83(5): 887–889.CrossRefGoogle Scholar
  8. Colautti R I, Macisaac H J, Macisaac H J. 2004. A neutral terminology to define ‘invasive’ species. Diversity and Distributions, 10(1): 135–141.CrossRefGoogle Scholar
  9. Dainese M, Leps J, de Belo F. 2015. Different effects of elevation, habitat fragmentation and grazing management on the functional, phylogenetic and taxonomic structure of mountain grasslands. Perspectives in Plant Ecology, Evolution and Systematics, 17(1): 44–53.CrossRefGoogle Scholar
  10. Dawson W, Moser D, van Kleunen M, et al. 2017. Global hotspots and correlates of alien species richness across taxonomic groups. Nature Ecology and Evolution, doi: s41559-017-0186.Google Scholar
  11. Díaz S, Kattge J, Cornelissen J H, Wright I J, et al. 2016. The global spectrum of plant form and function. Nature, 529(7585): 167–171.CrossRefGoogle Scholar
  12. Evans J R, Poorter H. 2001. Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell and Environment, 24(8): 755–767.CrossRefGoogle Scholar
  13. Evert R F. 2013. Esau’s Plant Anatomy-Meristems, Cells, and Tissues of Tree Plant Body-their Structures, Function and Development (3rd ed.). New Jersey: John Wiley & Sons, Inc., 601.Google Scholar
  14. Fahn A. 1990. Plant Anatomy (2nd ed.). Oxford: Butterworth Heinemann, 611.Google Scholar
  15. Falcioni R, Moriwaki T, Bonato C M, et al. 2017. Distinct growth light and gibberellin regimes alter leaf anatomy and reveal their influence on leaf optical properties. Environmental and Experimental Botany, 140(1): 86–95.CrossRefGoogle Scholar
  16. Gil-Pelegrín E, Saz M A, Cuadrat J M, et al. 2017. Oaks under mediterranean-type climates: Functional response to summer aridity. In: Gil-Pelegrín E, Peguero-Pina, Sancho-Knapik D. Oaks Physiological Ecology. Exploring the Functional Diversity of Genus quercus L. Aragón, Zaragoza, Spain: Springer, 137–193.CrossRefGoogle Scholar
  17. Gotelli N J, Ellison A M. 2012. The analysis of multivariate. In: Gotelli N J, Ellison A M. A Primer of Ecological Statistics. Sunderland: Sinauer Associates, 383–406.Google Scholar
  18. Hassan L M, Galal T M, Farahat E A, et al. 2015. The biology of Calotropis procera (Aiton) W.T. Trees, 29(2): 311–320.CrossRefGoogle Scholar
  19. Husson F, Josse J, Le S, et al. 2017. FactoMineR: multivariate exploratory data analysis and data mining. R Development Core Team. [2019-05-13]. Scholar
  20. Kozlov M V, Cornelissen T, Gavrikov D E, et al. 2017. Reproducibility of fluctuating asymmetry measurements in plants: Sources of variation and implications for study design. Ecological Indicators, 73(1): 733–740.CrossRefGoogle Scholar
  21. Leigh A, Sevanto S, Close J D, et al. 2016. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant, Cell and Environment, 40(2): 237–248.CrossRefGoogle Scholar
  22. Lindorf H, Parisca L, Rodríguez P. 1991. Botanic: classification, structure and reproduction, Caracas. Venezuela: Universidad Central de Venezuela, 583. (in Spanish)Google Scholar
  23. Mehra J. 2001. Max planck and the law of blackbody radiation. In: Mehra J. The Golden Age of Theoretical Physics. Singapore: National Academies Press, 19–55.CrossRefGoogle Scholar
  24. Michaletz S T, Weiser M D, Zhou J, et al. 2015. Plant thermoregulation: Energetics, trait-environment interactions, and carbon economics. Trends in Ecology and Evolution, 30 (1): 714–724.CrossRefGoogle Scholar
  25. Møller A P, Eriksson M. 1994. Patterns of fluctuating asymmetry in flowers: implications for sexual selection in plants. Journal of Evolutionary Biology, 7(1): 97–113.CrossRefGoogle Scholar
  26. Møller A P. 1995. Leaf-mining insects and fluctuating asymmetry in elm Ulmus glabra leaves. Journal of Animal Ecology, 64 (6): 697–707.CrossRefGoogle Scholar
  27. Monk C D. 1966. An ecological significance of evergreenness. Ecology, 47(3): 504–505.CrossRefGoogle Scholar
  28. Muriira N G, Muchugi A, Yu A, et al. 2018. Genetic diversity analysis reveals genetic differentiation and strong population structure in Calotropis plants. Science Reports, 8(7832): 1–10.Google Scholar
  29. Nagel J M, Griffin K L. 2001. Construction cost and invasive potential: comparing Lythrum salicaria (Lythraceae) with co-occurring native species along pond banks. American Journal of Botany, 88(12): 2252–2258.CrossRefGoogle Scholar
  30. Pagnucco K S, Maynard G A, Fera S A, et al. 2015. The future of species invasions in the Great Lakes-St. Lawrence River basin. Journal of Great Lakes Research, 41(Suppl.1): 96–107.CrossRefGoogle Scholar
  31. Parkhurst D F, Loucks O L. 1972. Optimal leaf size in relation to environment. Journal of Ecology, 60(2): 505–537.CrossRefGoogle Scholar
  32. Parsons P A. 1992. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity, 68(4): 361–364.CrossRefGoogle Scholar
  33. Peguero-Pina J J, Sancho-Knapik D, Barrón E, et al. 2014. Morphological and physiological divergences within Quercus ilex support the existence of different ecotypes depending on climatic dryness. Annals of Botany, 114(1): 301–313.CrossRefGoogle Scholar
  34. Peguero-Pina J J, Sancho-Knapik D, Flexas J, et al. 2016a. Light acclimation of photosynthesis in two closely related firs (Abies pinsapo Boiss. and Abies alba Mill.): the role of leaf anatomy and mesophyll conductance to CO2. Tree Physiology, 36(3): 300–310.CrossRefGoogle Scholar
  35. Peguero-Pina J J, Sisó S, Fernández-Marín B, et al. 2016b. Leaf functional plasticity decreases the water consumption without further consequences for carbon uptake in Quercus coccifera L. under Mediterranean conditions. Tree Physiology, 36(3): 356–367.CrossRefGoogle Scholar
  36. Pompelli M F, Antunes W C, Ferreira D T R G, et al. 2012. Allometric models for non-destructive leaf area estimation of the Jatropha curcas. Biomass and Bioenergy, 36(1): 77–85.CrossRefGoogle Scholar
  37. Poorter H, Pepin S, Rijkers T, et al. 2006. Construction costs, chemical composition and payback time of high- and low-irradiance leaves. Journal of Experimental Botany, 57(2): 355–371.CrossRefGoogle Scholar
  38. Poorter H, Niinemets Ü, Poorter L, et al. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist, 182(1): 565–588.CrossRefGoogle Scholar
  39. Reich P B, Walters M B, Ellsworth D S. 1992. Leaf lifespan in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs, 62(3): 365–392.CrossRefGoogle Scholar
  40. Rivas R, Frosi G, Ramos D G, et al. 2017. Photosynthetic limitation and mechanisms of photoprotection under drought and recovery of Calotropis procera, an evergreen C3 from arid regions. Plant Physiology and Biochemistry, 118(1): 589–599.CrossRefGoogle Scholar
  41. Sant’anna-Neto J L, Galvani E, Vieira B C. 2015. Climates of Brazil: past and present. In: Vieira B, Salgado A, Santos L P. Landscapes and Landforms of Brazil. World Geomorphological Landscapes. Dordrecht: Springer, 33–41.Google Scholar
  42. Sharma B M. 1968. Root systems of some desert plants in Churu, Rajasthan. Indian Forester, 94(3): 240–246.Google Scholar
  43. Simberloff D, Martin J-L, Genovesi P, et al. 2012. Impacts of biological invasions: what's what and the way forward. Trends in Ecology and Evolution, 28(1): 58–66.CrossRefGoogle Scholar
  44. Singh G. 1995. An agroforestry practice for the development of salt lands using Prosopis juliflora and Leptochloa fusca. Agroforestry Systems, 29(1): 61–75.CrossRefGoogle Scholar
  45. Smith H L, McAusland L, Murchie E H. 2017. Don’t ignore the green light: exploring diverse roles in plant processes. Journal of Experimental Botany, 68(9): 2099–2110.CrossRefGoogle Scholar
  46. Souza G M, Viana J O F, Oliveira R F. 2005. Asymmetrical leaves induced by water deficit show asymmetric photosynthesis in common bean. Brazilian Journal of Plant Physiology, 17(2): 223–227.CrossRefGoogle Scholar
  47. Terashima I, Fujita T, Inoue T, et al. 2009. Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of qhy leaves are green. Plant and Cell Physiology, 50(4): 684–697.CrossRefGoogle Scholar
  48. Tezara W, Colombo R, Coronel I, et al. 2011. Water relations and photosynthetic capacity of two species of Calotropis in a tropical semi-arid ecosystem. Annals of Botany, 107(3): 397–405.CrossRefGoogle Scholar
  49. Thakur S, Sidhu M C. 2017. Medicinal plant remedies for dermatological problems. Current Botany, 8(1): 23–33.Google Scholar
  50. Valladares F, Balaguer L, Martinez-Ferri E, et al. 2002. Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phytologist, 156(3): 457–467.CrossRefGoogle Scholar
  51. Villar R, Ruiz-Robleto J, Ubera J L, et al. 2013. Exploring variation in leaf mass per area (LMA) from leaf to cell: an anatomical analysis of 26 woody species. American Journal of Botany, 100(10): 1969–1980.CrossRefGoogle Scholar
  52. Wang C, Zhao C Y, Xu Z, et al. 2013. Effect of vegetation on soil water retention and storage in a semi-arid alpine forest catchment. Journal of Arid Land, 5(2): 207–219.CrossRefGoogle Scholar
  53. Wei T, Simko V. 2016. An introduction to corrplot Package. R Development Core Team. [2019-05-13]. Scholar
  54. White J W, Montes R C. 2005. Variation in parameters related to leaf thickness in common bean (Phaseolus vulgaris L.). Field Crops Research, 91(1): 7–21.CrossRefGoogle Scholar
  55. Witkowski E T, Lamont B B. 1991. Leaf specific mass confounds leaf density and thickness. Oecologia, 88(4): 486–493.CrossRefGoogle Scholar
  56. Wright I J, Reich P B, Westoby M, et al. 2004. The worldwide leaf economics spectrum. Nature, 428(6985): 821–827.CrossRefGoogle Scholar

Copyright information

© Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Marcelo F. Pompelli
    • 1
    Email author
  • Keila R. Mendes
    • 1
  • Marcio V. Ramos
    • 2
  • José N. B. Santos
    • 1
  • Diaa T. A. Youssef
    • 3
  • Jaqueline D. Pereira
    • 4
  • Laurício Endres
    • 5
  • Alfredo Jarma-Orozco
    • 6
  • Rodolfo Solano-Gomes
    • 7
  • Betty Jarma-Arroyo
    • 6
  • André L. J. Silva
    • 5
  • Marcos A. Santos
    • 1
  • Werner C. Antunes
    • 8
  1. 1.Plant Physiology Laboratory, Department of BotanyFederal University of PernambucoRecifeBrazil
  2. 2.Department of Biochemistry and Molecular BiologyFederal University of CearáFortalezaBrazil
  3. 3.Department of Natural Products, Faculty of PharmacyKing Abdulaziz UniversityJeddahSaudi Arabia
  4. 4.Institute of BotanyFederal University of ViçosaRio ParanaibaBrazil
  5. 5.Plant Ecophysiology LaboratoryFederal University of AlagoasMaceioBrazil
  6. 6.Faculty of Agricultural ScienceUniversity of CórdobaMonteríaColombia
  7. 7.Instituto Politécnico NacionalResearch Interdisciplinary Center for Integrated Rural DevelopmentSanta Cruz Xoxocotlan, OaxacaMexico
  8. 8.Department of BiologyUniversity of MaringáMaringáBrazil

Personalised recommendations