ía Mesoamericana ISSN electrónico: 2215-3608

Crop physiological responses to high temperature stress. I. Molecular, biochemical and physiological aspects.

Néstor Felipe Chaves-Barrantes, Marco Vinicio Gutiérrez-Soto



The objective of this review was to integrate the mechanisms by which plants respond to high temperature stress along the soil-plant-atmosphere continuum, from an agronomic perspective. The review presents the physiological basis underlying thermal stress, for which the optimum and threshold temperatures of crops are examined, along with methodologies for its study and the molecular, biochemical and physiological responses of plants to high temperature. The effects of high temperatures on cell ultrastructure and metabolism, respiration, the acclimation of Q10, membrane stability, accumulation of compatible osmolites, production of pigments, secondary metabolites and stress proteins, production of reactive oxygen species (ROS) and antioxidant enzymes, and the effects on photosynthesis and assimilate partitioning are examined. Hormonal changes and signaling regulating plant responses in the eld, and the acclimation to temperature stress are also discussed. 


antioxidant enzymes, compatible osmolites, heat shock proteins, induced thermo-tolerance.


Agustí, M. 2004. Fruticultura. Mundi Prensa, ESP.

Almeselmani, M., P.S. Deshmukh, R.K. Sairam, S.R. Kushwaha, and T.P. Singh. 2006. Protective role of antioxidant enzymes under high temperature stress.

Plant Sci. 171:382-388.

Alvarado, M., y G. Rojas. 2007. El cultivo y bene ciado del café. Segunda reimpresión. EUNED, San José, CRC.

Alves, A.A. 2002. Cassava botany and physiology. In: R.J. Hillocks et al., editors, Cassava: biology, production and utilization. CAB Int., Wallingford, GBR. p. 67-89.

Ashraf, M., and M.R. Foolad. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59:206-216.

Atkin, O.K., and M.K. Tjoelker. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci. 8:343-351.

Baena-González, E., F. Rolland, J.M. Thevelein, and J. Sheen. 2007. A central integrator of transcription networks in plant stress and energy signaling. Nature 448:938-943.

Banowetz, G.M., K. Ammar, and D.D. Chen. 1999. Temperature effects on cytokinin accumulation and kernel mass in a dwarf wheat. Ann. Bot. 83:303-307.

Barnabás, B., K. Jäger, and A. Fehér. 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 31:11-38.

Barrios, E.J., y C. López. 2009. Temperatura base y tasa de extensión foliar en frijol. Agrociencia 43:29-35.

Berry, J.A., and J.K. Raison. 1981. Responses of macrophytes to temperature. In: O.L. Lange et al., editors, Physiological plant ecology. Vol. 12A. Responses to the physical environment. Springer-Verlag, Berlin, GER. p. 277-338.

Bilger, H.W., U. Schreiber, and O.L. Lange. 1984. Determination of leaf heat resistance: comparative investigation of chlorophyll uorescence changes and tissue necrosis methods. Oecol. 63:256-262.

Blum, A. 1988. Plant breeding for stress environments. CRC Press Inc., Boca Raton, F.L., USA.

Boote, K.J., L.H. Allen, P.V. Prasad, J.T. Baker, R.W. Gesch, A.M. Snyder, D. Pan, and J.M. Thomas. 2005. Elevated temperature and CO2 impacts on pollination, reproductive growth, and yield of several globally important crops. J. Agric. Meteorol. 60:469-474.

Campostrini, E., and D.M. Glenn. 2007. Ecophysiology of papaya: a review. Braz. J. Plant Physiol. 19:413-424.

Castro, S., V.H. Ramos, y A.J. Huerta. 2012. Uso de la termoestabilidad de la membrana celular para la estimación de la tolerancia al calor en maíz. Interciencia (Venezuela) 37:921-926.

Challinor, A.J., T.R. Wheeler, P.Q. Craufurd, C.A. Ferro, and D.B. Stephenson. 2007. Adaptation of crops to climate change through genotypic responses to mean and extreme temperatures. Agric. Ecosyst. Environ. 119:190-204.

Cheikh, N., and R.J. Jones. 1994. Disruption of maize kernel growth and development by heat stress. Role of cytoki- nin/abscisic acid balance. Plant Physiol. 106:45-51.

Chen, H.H., Z.Y. Shen, and P.H. Lee. 1982. Adaptability of crop plants to high temperature stress. Crop Sci. 22:719-725.

Conde, A., M.M. Chaves, and H. Gerós. 2011. Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 52:1583-1602.

Corley, R.H.V. 1983. Potential productivity of tropical perennial crops. Exp. Agr. 19:217-237.

Corley, R., y P. Tinker. 2009. La palma de aceite. 4a ed. Federación Nacional de Palma de Aceite (FEDEPALMA) y Blackwell Publishing Company, Bogotá, COL.

Crafts, S.J., and M.E. Salvucci. 2002. Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol. 129:1773-1780.

Cronjé, M.J., and L. Bornman. 1999. Salicylic acid in uences Hsp70/Hsc70 expression in Lycopersicon esculentum: dose- and time-dependent induction or potentiation. Biochem. Biophys. Res. Commun. 265:422-427.

Cronjé, M.J., I.E. Weir, and L. Bornman. 2004. Salicylic acid- mediated potentiation of Hsp70 induction correlates with reduced apoptosis in tobacco protoplasts. Cytometry 61A:76-87.

Da Matta, F.M., and J.D. Ramalho. 2006. Impacts of drought and temperature stress on coffee physiology and production: a review. Braz. J. Plant Physiol. 18:55-81.

Dat, J.F., H. Lopez, C.H. Foyer, and I.M. Scott. 2000. Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J. Plant Physiol. 156:659-665.

Dietze, M.C., A. Sala, M.S. Carbone, C.I. Czimczik, J.A. Mantooth, A.D. Richardson, and R. Vargas. 2013. Nonstructural carbon in woody plants. Annu. Rev. Plant Biol. 65:667-687.

Downs, C.A., K.E. McDougall, C.M. Woodley, J.E. Fauth, R.H. Richmond, A. Kushmaro, S.W. Gibb, Y. Loya, G.K. Ostrander, and E. Kramarsky-Winter. 2013. Heat-stress and light-stress induce different cellular pathologies in the symbiotic dino agellate during coral bleaching. PLOS One 8:e77173. doi:10.1371/journal.pone.0077173

Dreher K., and J. Callis. 2007. Ubiquitin, hormones and biotic stress in plants. Ann. Bot. 99:787-822.

Easterling, D.R., B. Horton, P.D. Jones, T.C. Peterson, T.R. Karl, D.E. Parker, M.J. Salinger, V. Razuvayev, N. Plummer, P. Jamason, and C.K. Folland. 1997. Maximum and minimum temperature trends for the globe. Sci. 277:364-367.

Firon, N., E. Pressman, S. Meir, R. Khoury, and L. Althan. 2012. Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants 2012:pls024. doi:10.1093/aobpla/pls024.

Fischer, G., F. Casierra, y W. Piedrahíta. 2009. Eco siología de las especies pasi oráceas en Colombia. En: D. Miranda et al., editores, Cultivo, poscosecha y comercialización de las pasi oráceas en Colombia: maracuyá, granadilla, gulupa y curuba. Sociedad Colombiana de Ciencias Hortícolas, COL. p. 45-68.

Galán, V. 2009. El cultivo del mango. 2a ed. Mundi Prensa, Madrid, ESP.

Georgieva, K. 1999. Some mechanisms of damage and acclimation of the photosynthetic apparatus due to high temperature. Bulg. J. Plant Physiol. 25:89-99.

Gong, M., Y.J. Li, and S.Z. Chen. 1998. Abscisic acid- induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J. Plant Physiol. 153:488-496.

Gruber, B.D., R. Giehl, S. Friedel, and N. Von Wirén. 2013. Plasticity of the Arabidopsis root system under nutrient de ciencies. Plant Physiol. 163:161-179.

Haldimann, P., and U. Feller. 2005. Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves. Plant Cell Environ. 28:302-317.

Hsiao, T.C. 1973. Plant responses to water stress. Ann. Rev. Plant Physiol. 24:519-570.

Huberman, M., J. Riov, B. Aloni, and R. Goren. 1997. Role of ethylene biosynthesis and auxin content and transport in high temperature-induced abscission of pepper reproductive organs. J. Plant Growth Regul. 16:129-135.

Iba, K. 2002. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu. Rev. Plant Biol. 53:225-245.

Jagadish, S.V.K., P.Q. Craufurd, and T.R. Wheeler. 2007. High temperature stress and spikelet fertility in rice (Oryza sativa L.). J. Exp. Bot. 58:1627-1635.

Jagadish, S.V.K., R. Muthurajan, R. Oane, T.R.Wheeler, S. Heuer, J. Bennett, and P.Q. Craufurd. 2010. Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J. Exp. Bot. 61:143-156.

Jones, P.D., and A. Moberg. 2003. Hemispheric and large- scale surface air temperature variations: an extensive revision and an update to 2001. J. Climate 16:206-223.

Jones, H.G., and R.A. Vaughan. 2010. Remote sensing of vegetation. Principles, techniques and applications. Oxford University Press, N.Y., USA.

Kappen, L. 1981. Ecological signi cance of resistance to high temperature. In: O.L. Lange et al., editors, Physiological plant ecology. Vol. 12A. Responses to the physical environment. Springer-Verlag, Berlin, GER. p. 439-474.

Karademir, E., C. Karademir, R. Ekinci, S. Basba, and H. Basal. 2012. Screening cotton varieties (Gossypium hirsutum L.) for heat tolerance under eld conditions. Afr. J. Agric. Res. 7:6335-6342.

Kavi-Kishor, P.B., S. Sangam, R.N. Amrutha, P. Sri Laxmi, K.R. Naidu, K.R.S.S. Rao, S. Rao, K.J. Reddy, P. Theriappan, and N. Sreenivasulu. 2005. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr. Sci. 88:424-438.

Kotak, S., J. Larkindale, U. Lee, P. Von Koskull, E. Vierling, and K.D. Scharf. 2007. Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10:310-316.

Kurek, I., T.K. Chang, S.M. Bertain, A. Madrigal, L. Liu, M.W. Lassner, and G. Zhu. 2007. Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19:3230-3241.

Laf te, H.R. 2001. Fisiología del maíz tropical. En: R.L. Paliwal et al., editores, El maíz en los trópicos. Mejoramiento y producción. FAO, Roma, ITA. p. 21-28.

Larcher, W. 1980. Physiological plant ecology. 2 ed. Springer-Verlag, Berlin, GER.

Larkindale, J., J.D. Hall, M.R. Knight, and E. Vierling. 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138: 882–897.

Larkindale, J., and M.R. Knight. 2002. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene and salicylic acid. Plant Physiol. 128:682-695.

Ledesma, N.A., M. Nakata, and N. Sugiyama. 2008. Effect of high temperature stress on the reproductive growth of strawberry cvs. Nyoho and Toyonoka. Sci. Hort. 116:186-193.

Levitt, J. 1980. Responses of plants to environmental stresses. Vol. I. Chilling, freezing, and high temperature stress. 2nd ed. Academic Press, N.Y., USA.

López, H., J.F. Dat, C.H. Foyer, and I.M. Scott. 1998. Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2O2. J. Exp. Bot. 49:713-720.

Long, S.P., and D.R. Ort. 2010. More than taking the heat: crops and global change. Curr. Opin. Plant Biol. 13:241-248.

Los, D.A., and N. Murata. 2004. Membrane uidity and its roles in the perception of environmental signals. BBA- Biomembranes 1666:142-157.

Maestri, E., N. Klueva, C. Perrotta, M. Gulli, T. Nguyen, and N. Marmiroli. 2002. Molecular genetics of heat tolerance and heat shock proteins in cereals. J. Plant Mol. Biol. 48:667-681.

Maroto, J. 1990. Elementos de horticultura general. Especialmente aplicada al cultivo de plantas de consistencia herbácea. Mundi Prensa, Madrid, ESP.

Mittler, R. 2002. Oxidative stress; antioxidants and stress tolerance. Trends Plant Sci. 7:405-410.

Murata, Y., I. Mori, and S. Munemasa. 2015. Diverse stomatal signaling and the signal integration mechanism. Ann. Rev. Plant Biol. 66:369-392.

Nagai, T., and A. Makino. 2009. Differences between rice and wheat in temperature responses of photosynthesis and plant growth. Plant Cell Physiol. 50:744-755.

Nagesh, R., and V.R. Devaraj. 2008. High temperature and salt stress response in French bean (Phaseolus vulgaris). Aust. J. Crop Sci. 2:40-48.

Nakagawa, H., and T. Horie. 2000. Rice responses to elevated CO2 and temperature. Global Environ. Res. 2:101-113.

Nakasone, H.Y., and R.E. Paull. 2004. Tropical fruits. 2nd ed. CAB Int., Wallimngford, GBR.

Omae, H., A. Kumar, and M. Shono. 2012. Adaptation to high temperature and water de cit in the common bean (Phaseolus vulgaris L.) during the reproductive period. J. Bot. Article ID 803413 doi:10.1155/2012/803413.

Osorio, G. 2007. Manual técnico. Buenas prácticas agrícolas –BPA– y buenas prácticas de manufactura –BPM– en la producción de caña y panela. FAO, MANA y CORPOICA, Medellín, COL.

Pareek, A., S.L. Singla, and A. Grover. 1997. Short-term salinity and high temperature stress-associated ultrastructural alterations in young leaf cells of Oryza sativa L. Ann. Bot. 80:629-639.

Parent, B., and F. Tardieu. 2012. Temperature responses of developmental processes have not been affected by breeding in different ecological areas for 17 crop species. New Phytol. 194:760-774.

Park, E.J., Z. Jeknić, and T.H. Chen. 2006. Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol. 47:706-714.

Pimentel, C., C. Bernacchi, and S. Long. 2007. Limitations to photosynthesis at different temperatures in the leaves of Citrus limon. Braz. J. Plant Physiol. 19:141-147.

Porch, T.G., and A.E. Hall. 2013. Heat tolerance. In: C. Kole, editor, Genomics and breeding for climate-resilient crops. Vol. 2. Springer-Verlag, Berlin, GER. p. 167-202.

Porch, T.G., and M. Jahn. 2001. Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris. Plant Cell Environ. 24:723-731.

Porter, J.R. 2005. Rising temperatures are likely to reduce crop yields. Nature 436:174. doi:10.1038/436174b

Prasad, P.V., K.J. Boote, L.H. Allen Jr., and J.M. Thomas. 2002. Effects of elevated temperature and carbon dioxide on seed-set and yield of kidney bean (Phaseolus vulgaris L.). Glob. Change Biol. 8:710-721.

Prasad, P.V., K.J. Boote, L.H. Allen Jr., J.E. Sheehy, and J.M. Thomas. 2006. Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Res. 95:398-411.

Prasad, P.V., P.Q. Craufurd, and R.J. Summer eld. 2000. Effect of high air and soil temperature on dry matter production, pod yield and yield components of groundnut. Plant Soil 222:231-239.

Qiu, N., and C. Lu. 2003. Enhanced tolerance of photosynthesis against high temperature damage in salt- adapted halophyte Atriplex centralasiatica plants. Plant Cell Environ. 26:1137-1145.

Quan, R., M. Shang, H. Zhang, Y. Zhao, and J. Zhang. 2004. Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotech. J. 2:477-486.

Rahman, H.U., S.A. Malik, and M. Saleem. 2004. Heat tolerance of upland cotton during the fruiting stage evaluated using cellular membrane thermostability. Field Crops Res. 85:149-158.

Rosenberg, N.J., B.L. Blad, and S.B. Verma. 1983. Microclimate: the biological environment. 2nd ed. John Wiley & Sons, N.Y., USA.

Ruiz, J.A., H.E. Flores, J.L. Ramírez, y D.R. González. 2002. Temperaturas cardinales y duración del ciclo de madurez del híbrido de maíz H-311 en condiciones de temporal. Agrociencia 36:569-577.

Sadras, V.O., and R.A. Richards. 2014. Improvement of crop yield in dry environments: benchmarks, levels of organization and the role of nitrogen. J. Exp. Bot. 65:1981-1985.

Sakamoto, A., and N. Murata. 2002. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25:163-171.

Salvucci, M.E., and S.J. Crafts. 2004. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol. Plant. 120:179-186.

Samach, A., and P.A. Wigge. 2005. Ambient temperature perception in plants. Curr. Opin. Plant Biol. 8:483-486.

Savchenko, G.E., E.A. Klyuchareva, L.M. Abrabchik, and E.V. Serdyuchenko. 2002. Effect of periodic heat shock on the membrane system of etioplasts. Russ. J. Plant Physiol. 49:349-359.

Schwacke, R., S. Grallath, K.E. Breitkreuz, E. Stransky, H. Stransky, W.B Frommer, and D. Rentscha. 1999. LeProT1, a transporter for proline, glycine betaine, and g-amino butyric acid in tomato pollen. Plant Cell 11:377-391.

Sevanto, S. 2014. Phloem transport and drought. J. Exp. Bot. 65:1751-1759.

Sharkey, T.D. 2005. Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ. 28:269-277.

Shi, Q., Z. Bao, Z. Zhu, Q. Ying, and Q. Qian. 2006. Effects of different treatments of salicylic acid on heat tolerance, chlorophyll uorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul. 48:127-135.

Smalle, J., and R.D. Vierstra. 2004. The ubiquitine 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55:555-590.

Snyman, M., and M.J. Cronjé. 2008. Modulation of heat shock factors accompanies salicylic acid-mediated potentiation oh Hsp70 in tomato seedlings. J. Exp. Bot. 59:2125-2132.

Soler, J., y G. Soler. 2006. Cítricos. Variedades y técnicas de cultivo. Mundi Prensa, ESP.

Subirós, F. 2000. El cultivo de la caña de azúcar. Primera reimpresión. EUNED, San José, CRC.

Sung, D.Y., F. Kaplan, K.J. Lee, and C.L. Guy. 2003. Acquired tolerance to temperature extremes. Trends Plant Sci. 8:179-187.

Suzuki, K., T. Tsukaguchi, H. Takeda, and Y. Egawa. 2001. Decrease of pollen stainability of green bean at high temperatures and relationship to heat tolerance. J. Amer. Soc. Hort. Sci. 126:571-574.

Szabados, L., and A. Savouré. 2010. Proline: a multifunctional amino acid. Trends Plant Sci. 15:89-97.

Taiz, L., and E. Zeiger. 2006. Plant Physiology. 4th edition. Sinauer Associates Inc., Sunderland, M.A., USA.

Taub, D.R., J.R. Seemann, and J.S. Coleman. 2000. Growth in elevated CO2 protects photosynthesis against high- temperature damage. Plant Cell Environ. 23:649-656.

Ulukan, H. 2008. Agronomic adaptation of some eld crops: a general approach. J. Agron. Crop Sci. 194:169-179.

Vallejo, F.A., y E.I. Estrada. 2004. Producción de hortalizas de clima cálido. Universidad Nacional de Colombia Sede Palmira, Cali, COL.

Veerasamy, M., Y. He, and B. Huang. 2007. Leaf senescence and protein metabolism in creeping bentgrass exposed to heat stress and treated with cytokinins. J. Am. Soc. Hort. Sci. 132:467-472.

Verbruggen, N., and C. Hermans. 2008. Proline accumulation in plants: a review. Amino Acids 35:753-759.

Vettakkorumakankav, N.N., D. Falk, P. Saxena, and R.A. Fletcher. 1999. A crucial role for gibberellins in stress protection of plants. Plant Cell Physiol. 40:542-548.

Wahid, A. 2007. Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum of cinarum) sprouts. J. Plant Res. 120:219-228.

Wahid, A., and T.J. Close. 2007. Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol. Plant. 51:104-109.

Wahid, A., S. Gelani, M. Ahsraf, and M.R. Fooland. 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61:199-223.

Wang, W., B. Vinocur, O. Shoseyov, and A. Altman. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9:244-252.

Wang, L.C., M.C. Tsai, K.Y. Chang, Y.S. Fan, C.H. Yeh, and S.J. Wu. 2011. Involvement of the Arabidopsis HIT1/AtVPS53 tethering protein homologue in the acclimation of the plasma membrane to heat stress. J. Exp. Bot. 62:3609-3620.

Wang, S.Y., and W. Zheng. 2001. Effect of plant growth temperature on antioxidant capacity in strawberry. J. Agric. Food Chem. 49:4977-4982.

Wheeler, T.R., P.Q. Craufurd, R.H. Ellis, J.R. Porter, and P.V. Prasad. 2000. Temperature variability and the yield of annual crops. Agric. Ecosyst. Environ. 82:159-167.

White, J. 1985. Conceptos básicos de siología de frijol. En: M. López et al., editores, Frijol: investigación y producción. Centro Internacional de Agricultura Tropical (CIAT), Cali, COL. p. 43-60.

Wilhelm, E.P., R.E. Mullen, P.L. Keeling, and G.W. Singletary. 1999. Heat stress during grain lling in maize: effects on kernel growth and metabolism. Crop Sci. 39:1733-1741.

Xu, S., J. Li, X. Zhang, H. Wei, and L. Cui. 2006. Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ. Exp. Bot. 56:274-285.

Yang, X., Z. Liang, and C. Lu. 2005. Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol. 138:2299-2309.

Yeh, D.M., and H.F. Lin. 2003. Thermostability of cell membranes as a measure of heat tolerance and relationship to owering delay in chrysanthemum. J. Amer. Soc. Hort. Sci. 128:656-660.

Zinn, K.E., M. Tunc, and J.F. Harper. 2010. Temperature stress and plant sexual reproduction: uncovering the weakest links. J. Exp. Bot. 61:1959-1968.


  • There are currently no refbacks.

© 2017 Universidad de Costa Rica. Para ver más detalles sobre la distribución de los artículos en este sitio visite el aviso legal. Este sitio es desarrollado por UCRIndex y Open Journal Systems.