Keywords
leaf area
mangroves
tree height
stomatal densities
water stress.
altura
área foliar
densidad estomática
estrés hídrico
manglar
plasticidad de hoja
How to Cite
Abstract
In community ecology, the knowledge of abiotic factors, that determine intraspecific variability in ecophysiological and functional traits, is important for addressing major questions, such as plant community assembly and ecosystem functioning. Mangroves have several mechanisms of resistance to salinity and most species exhibit some xeromorphic features in order to conserve water. Leaf area and stomatal density play an important role in maintaining water balance, and gas exchange is regulated by their aperture and density, two traits that vary intraspecifically in response to environmental conditions, such as water stress and salinity. In this study, we evaluated the effects of salinity on stomatal density, leaf area and plant size in R. mangle and we tested for associations among the three variables, across three sites along a natural salinity gradient in the Xel-Há Park, Quintana Roo, Mexico. We hypothesized that high salinity sites would produce smaller plants, with smaller leaves, and fewer stomata. Three sampling sites with different environmental conditions were chosen and salinities were monitored monthly. A total of 542 plants were tagged and tree heights and diameters were measured for each individual within each of the three sampling sites. Three leaves from 20 trees from each site were measured to determine leaf area. Stomatal densities were determined in each leaf using nail polish casts, examining ten 1 mm squares per leaf under an optical microscope. A principal component analysis was used to assess association between tree height, leaf area, and stomatal density for each plot. The salinity gradient was reflected in plant size, producing smaller plants at the higher salinity site. The largest leaves were found at the low salinity site (51.2 ± 24.99 cm2). Leaf length was not correlated to plant size (LL vs. tree height: r= 0.02, P= 0.8205; LL vs. trunk diameter: r= 0.03, P= 0.7336), so we concluded that leaf length is an environmentally plastic trait of red mangroves that may vary as a function of environmental conditions, such as hydric stress caused by elevated salinity. The larger leaves from the low salinity site had lower densities of stomata (65.0 stomata.mm2 SD= 12.3), and increasing salinities did not decrease stomatal density (intermediate salinity site: 73.4 stomata.mm2 SD= 13.5; high salinity site: 74.8 stomata.mm2 SD= 17.3). Our results confirm that stomatal density is inversely related to leaf area (r= -0.29, P < 0.001), especially leaf width (r= -0.31, P < 0.001), and that salinity may increase stomatal density by causing reduction of leaf size.References
Aasamaa, K., Sober, A., & Rahi, M. (2001). Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal of Plant Physiology, 28(8), 765-774.
Araujo, R. J., Jaramillo, J. C., & Snedaker, S. C. (1997). LAI and leaf size differences in two red mangrove forest types in South Florida. Bulletin of Marine Sciences, 60(3), 643-647.
Aziz, I., & Khan, M. A. (2001). Effect of seawater on the growth, ion content and water potential of Rhizophora mucronata Lam. Journal of Plant Research, 114(3), 369-373.
Ball, M. C. (1988). Ecophysiology of mangroves. Trees, 2(3), 129-142.
Ball, M. C., & Pidsley, S. M. (1995). Growth responses to salinity in relation to distribution of two mangrove species, Sonneratia alba and S. lanceolata, in northern Australia. Functional Ecology, 9(1), 77-85.
Barbien, G., Vallone, S., Orsini, F., Paradiso, R., De Pascale, S., Negre-Zakharov, F., & Maggio, A. (2012). Stomatal density and metabolic determinants mediate salt stress adaptation and water use efficiency in basil (Ocimum basilicum L.). Journal of Plant Physiology, 169(17), 1737-1746.
Beerling, D. J., & Kelly, C. K. (1997). Stomatal density responses of temperate wodland plants over the past seven decades of CO2 increase: A comparison of Salisbury (1927) with contemporary data. American Journal of Botany, 84(11), 1572-1583.
Brewer, C. A. (1992). Responses by stomata on leaves to microenvironmental conditions. In C. A. Goldman (Ed.), Tested Studies for Laboratory Teaching (pp. 67-75). Proceedings of the 13th Workshop/Conference of the Association for Biology Laboratory Education (ABLE).
Bristow, J. M., & Looi, A. (1968). Effects of carbon dioxide on the growth and morphogenisis of Marsilea. American Journal of Botany, 55(8), 884-889.
Canoy, M. J. (1975). Diversity and stability in a Puerto Rican Rhizophora mangle L. forest. In G. Walsh, S. C. Snedaker, & H. Teas (Eds.), Proceedings of International Symposium on Biology and Management of Mangroves (Vol. I., pp. 344-356). Gainesville, Florida: Institute for Food and Agricultural Science, University of Florida.
Ciha, A. J., & Brun, W. A. (1975). Stomatal size and frequency in soybeans. Crop Science, 15(3), 309-313.
Clough, B. F. (1984). Growth and salt balance of the mangroves Avicennia marina (Forsk.) Vierh. and Rhizophora stylosa in relation to salinity. Australian Journal Plant Physiology, 11(5), 419-430.
CONABIO (2009). Manglares de México: Extensión y distribución. Mexico City: Comisión Nacional para el conocimiento y uso de la biodiversidad.
Connor, D. J. (1969). Growth of grey mangrove (Avicennia marina) in nutrient culture. Biotropica, 1(2), 36-40.
Dahdouh-Guebas, F., De Bondt, R., Abesinghe, P. D., Kairo, J. G., Cannicci, S., Triest, L., & Koedam, N. (2004). Comparative study of the disjunct zonation pattern of the grey mangrove Avicennia marina (Forsk.) Vierh. in Gazi Bay (Kenya). Bulletin of Marine Science, 74(2), 237-252.
Das, S., & Ghose, M. (1993). Morphology of stomata and leaf hairs of some halophytes from Sundarbans, West Bengal. Phytomorphology, 43, 59-70.
Downton, W. J. S. (1982). Growth and osmotic relations of the mangrove Avicennia marina, as influenced by salinity. Functional Plant Biology, 9(5), 519-528.
Drake, P. L., Froend, R. H., & Franks, P. J. (2013). Smaller, faster stomata: Scaling of stomatal size, rate of response, and stomatal conductance. Journal of Experimental Botany, 64(2), 495-505.
Duke, J. A. (1983). Rhizophora mangle L. Handbook of Energy Crops. Retrieved from https://www.hort.purdue.edu/newcrop/duke_energy/Rhizophora_mangle.html
Ellison, A., Farnsworth, E., & Moore, G. (2015). Rhizophora mangle. The IUCN Red List of Threatened Species. Retrieved from http://www.iucnredlist.org/details/178851/0
Franks, P. J., & Farquhar, G. D. (2007). The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology, 143(1), 78-87.
Gay, A. P., & Hurd, R. G. (1975). The influence of light on stomatal density in the Tomato. New Phytology, 75(1), 37-46.
Hetherington, A. M., & Woodward, F. I. (2003). The role of stomata in sensing and driving environmental change. Nature, 424(6951), 901-908.
Hill, K. (2001). Rhizophora mangle, Smithsonian Marine Station Fort Pierce. Retrieved from http://www.sms.si.edu/irLspec/Rhizop_mangle.htm#reducing conditions.
Huner, N. P. A., Palta, J. P., Li, P. H., & Carter, J. V. (1981). Anatomical changes in leaves of Puma Rye in response to growth at cold-hardening temperatures. Botanical Gazette, 142, 55-62.
Hwang, Y. H., & Chen, S. C. (1995). Anatomical responses in Kandelia candel (L.) Druce seedlings growing in the presence of different concentrations of NaCl. Botanical Bulletin of Academia Sinica, 36, 181-188.
Krauss, K. W., & Allen, J. A. (2003). Influences of salinity and shade on seedling photosynthesis and growth of two mangrove species, Rhizophora mangle and Bruguiera sexangula, introduced to Hawaii. Aquatic Botany, 77(4), 311-324.
López Portillo, J., & Ezcurra, E. (2002). Los manglares de México: una revisión. Madera y Bosques, número especial, 27-51.
Lovelock, C. E., & Feller, I. C. (2003). Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest. Oecologia, 134(4), 455-62.
Lugo, A. E., Cintrón, G., & Goenaga, C. (1981). Mangrove ecosystems under stress. In W. Barrett & R. Rosenberg (Eds.), Stress Effects on Natural Ecosystems (pp. 129-153). Great Britain: John Wiley & Sons Ltd.
Lugo, A. E., & Snedaker, S. C. (1974). The ecology of mangroves. Annual Review of Ecology and Systematics, 5, 39-64.
Martínez, J. P., Silva, H., Ledent, J. F., & Pinto, M. (2007). Effect of drought stress on the osmotic adjustment, cell wall elasticity and cell volume of six cultivars of common beans (Phaseolus vulgaris L.). European Journal of Agronomy, 26(1), 30-38.
Medina, E., & Francisco, M. (1997). Osmolality and δ13C of leaf tissues of mangrove species from environments of contrasting rainfall and salinity. Estuarine, Coastal and Shelf Science, 45(3), 337-344.
Mehlig, U. (2006). Phenology of the red mangrove, Rhizophora mangle L., in the Caeté Estuary, Pará, equatorial Brazil. Aquatic Botany, 84(2), 158-164.
Orellana-Lanza, R., Espadas, C., Conde, C., & Gay, C. (2009). Atlas. Escenarios de cambio climático en la Península de Yucatán. Mérida, Yucatán, Mexico: Centro de Investigación Científica de Yucatán, A.C.
Organismo de cuenca Península de Yucatán. (2008). Cuerpo de agua denominado caleta Xel-Há, localizado en el estado de Quintana Roo (Informe técnico). México: Organismo de cuenca Península de Yucatán.
Pääkkönen, E., Vahala, J., Pohjolal, M., Holopainen, T., & Kärenlampi, L. (1998). Physiological, stomatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress. Plant, Cell & Environment, 21(7), 671-684.
Parida, A. K., Das, A. B., & Mittra, B. (2004). Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees - Structure and Function, 18(2), 167-174.
Pearce, D. W., Millard, S., Bray, D. F., & Rood, S. B. (2005). Stomatal characteristics of riparian poplar species in a semi-arid environment. Tree Physiology, 26(2), 211-218.
Quarrie, S. A., & Jones, H. G. (1977). Effects of abscisic acid and water stress on development and morphology of wheat. Journal of Experimental Botany, 28(1), 192-203.
Romero-Aranda, R., Soria, T., & Cuartero, J. (2001). Tomato plant-water uptake and plant-water relationships under saline growth conditions. Plant Science, 160(6), 265-272.
Saenger, P. (2002). Mangrove Ecology, Silviculture and Conservation. Dordrecht, The Netherlands: Kluwer Academic Publishers.
Salisbury, E. J. (1928). On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philosophical Transaction of the Royal Society of London, Series B, 216, 1-65.
Sam, O., Jeréz, E., Dell’Amico, J., & Ruiz-Sanchez, M. C. (2000). Water stress induced changes in anatomy of tomato leaf epidermes. Biologia Plantarum, 43(2), 275-277.
Schwarzbachl, A. E., & Ricklefs, R. E. (2001). The use of molecular data in mangrove plant research. Wetlands, Ecology and Management, 9(3), 195-201.
Siefert, A., Violle, C., Chalmandrier, L., Albert, C. H., Taudiere, A., Fajardo, A., Aarssen, L. W., …, & Wardle, D. A. (2015). A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters, 18(12), 1406-1419.
Snedaker, S. C., & Brown, M. S. (1981). Water quality and mangrove ecosystem dynamics. EPA-600/4-8 1-002. Florida, USA: United States Environmental Protection Agency, Gulf Breeze.
Spence, R. D., Wu, H., Sharpe, P. J. H., & Clark, K. G. (1986). Water stress effects on guard cell anatomy and the mechanical advantage of the epidermal cells. Plant, Cell & Environment, 9(3), 197-202.
Suárez, N., & Medina, E. (2005). Salinity effect on plant growth and leaf demography of the mangrove, Avicennia germinans L. Trees, 19(6), 722-728.
Tomlinson, P. B. (1986). The botany of mangroves. Cambrige: Cambridge University Press.
Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. A., & Wright, I. J. (2002). Plant ecological strategies: Some leading dimensions of variation between species. Annual Review of Ecology and Systematics, 33, 125-159.
Woodward, F. I., & Bazzaz, F. A. (1988). The Responses of stomatal density to CO2 partial pressure. Journal of Experimental Botany, 39(12), 1771-1781.
Xu, Z., & Zhou, G. (2008). Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. Journal of Experimental Botany, 59(12), 3317-25.
Zhang, Y., Zheng, Q., & Tyree, M. T. (2012). Factors controlling plasticity of leaf morphology in Robinia pseudoacacia L. I: height-associated variation in leaf structure. Annals of Forest Science, 69, 29-37.
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