Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-20T13:22:04.426Z Has data issue: false hasContentIssue false

Plant carbon and water fluxes in tropical montane cloud forests

Published online by Cambridge University Press:  15 July 2016

Sybil G. Gotsch*
Affiliation:
Department of Biology, Franklin and Marshall College, Lancaster, PA, USA
Heidi Asbjornsen
Affiliation:
Department of Natural Resources and the Environment, University of New Hampshire, Durham, NH, USA
Gregory R. Goldsmith
Affiliation:
Ecosystem Fluxes Group, Laboratory for Atmospheric Chemistry, Paul Scherrer Institut, Villigen, Switzerland
*
1Corresponding author. Email: sybil.gotsch@fandm.edu

Abstract:

Tropical montane cloud forests (TMCFs) are dynamic ecosystems defined by frequent, but intermittent, contact with fog. The resultant microclimate can vary considerably over short spatial and temporal scales, affecting the ecophysiology of TMCF plants. We synthesized research to date on TMCF carbon and water fluxes at the scale of the leaf, plant and ecosystem and then contextualized this synthesis with tropical lowland forest ecosystems. Mean light-saturated photosynthesis was lower than that of lowland forests, probably due to the effects of persistent reduced radiation leading to shade acclimation. Scaled to the ecosystem, measures of annual net primary productivity were also lower. Mean rates of transpiration, from the scale of the leaf to the ecosystem, were also lower than in lowland sites, likely due to lower atmospheric water demand, although there was considerable overlap in range. Lastly, although carbon use efficiency appears relatively invariant, limited evidence indicates that water use efficiency generally increases with altitude, perhaps due to increased cloudiness exerting a stronger effect on vapour pressure deficit than photosynthesis. The results reveal clear differences in carbon and water balance between TMCFs and their lowland counterparts and suggest many outstanding questions for understanding TMCF ecophysiology now and in the future.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALTON, P. B. 2008. Reduced carbon sequestration in terrestrial ecosystems under overcast skies compared to clear skies. Agricultural and Forest Meteorology 148:16411653.Google Scholar
ALVARADO-BARRIENTOS, M. S., HOLWERDA, F., ASBJORNSEN, H., DAWSON, T. E. & BRUIJNZEEL, L. A. 2014. Suppression of transpiration due to cloud immersion in a seasonally dry Mexican weeping pine plantation. Agricultural and Forest Meteorology 186:1225.Google Scholar
ATAROFF, M. & RADA, F. 2000. Deforestation impact on water dynamics in a Venezuelan Andean cloud forest. Ambio 29:440444.Google Scholar
BENNER, J. W. & VITOUSEK, P. M. 2011. Cyanolichens: a link between the phosphorus and nitrogen cycles in a Hawaiian montane forest. Journal of Tropical Ecology 28:7381.Google Scholar
BERRY, Z. C., GOTSCH, S. G., HOLWERDA, F., MUÑOZ-VILLERS, L. E. & ASBJORNSEN, H. 2016. Slope position influences vegetation-atmosphere interactions in a tropical montane cloud forest. Agricultural and Forest Meteorology 221:207218.Google Scholar
BONAL, D., BORN, C., BRECHERT, C., COSTE, S., MARCON, E., ROGGY, J. C. & GUEHL, J. M. 2007. The successional status of tropical rainforest tree species is associated with differences in leaf carbon isotope discrimination and functional traits. Annals of Forest Science 64:169176.Google Scholar
BONAL, D., PONTON, S., LE THIEC, D., RICHARD, B., NINGRE, N., HÉRAULT, B., OGÉE, J., GONZALEZ, S., PIGNAL, M., SABATIER, D. & GUFHI, J.-M. 2011. Leaf functional response to increasing atmospheric CO2 concentrations over the last century in two northern Amazonian tree species: a historical δ13C and δ18O approach using herbarium samples. Plant, Cell and Environment 34:13321334.Google Scholar
BRUIJNZEEL, L. A. & HAMILTON, L. S. 2000. Decision time for cloud forests. IHP Humid Tropics Programme Series No. 13, UNESCO Division of Water Sciences, Paris. 41 pp.Google Scholar
BRUIJNZEEL, L. A. & VENEKLAAS, E. J. 1998. Climatic conditions and tropical montane cloud forest productivity: the fog has not lifted yet. Ecology 79:39.Google Scholar
BRUIJNZEEL, L. A., SCATENA, F. N. & HAMILTON, L. S. (eds). 2010. Tropical montane cloud forests: science for conservation and management. Cambridge University Press, Cambridge. 768 pp.Google Scholar
BRUIJNZEEL, L. A., MULLIGAN, M. & SCATENA, F. N. 2011. Hydrometeorology of tropical montane cloud forests: emerging patterns. Hydrological Processes 25:465498.Google Scholar
BUCCI, S. J., SCHOLZ, F. G., GOLDSTEIN, G., MEINZER, F. C., HINOJOSA, J. A., HOFFMANN, W. A. & FRANCO, A. C. 2004. Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiology 24:11191127.Google Scholar
BURGESS, S. S. O. & DAWSON, T. E. 2004. The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant Cell and Environment 27:10231034.Google Scholar
CAVELIER, J. 1990. Tissue water relations in elfin cloud forest tree species of Serrania de Macuira, Guajira, Colombia. Trees – Structure and Function 4:155163.Google Scholar
CERNUSAK, L. A., ARANDA, J., MARSHALL, J. D. & WINTER, K. 2007. Large variation in whole-plant water-use efficiency among tropical tree species. New Phytologist 173:294305.Google Scholar
CERNUSAK, L. A., WINTER, K., DALLING, J. W., HOLTUM, J. A. M., JARAMILLO, C., KORNER, C., LEAKEY, A. D. B., NORBY, R. J., POULTER, B., TURNER, B. L. & WRIGHT, S. J. 2013. Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. Functional Plant Biology 40:531551.Google Scholar
CHAVE, J., NAVARRETE, D., ALMEIDA, S., ALVAREZ, E., ARAGÃO, L. E. O. C., BONAL, D., CHÂTELET, P., SILVA-ESPEJO, J. E., GORET, J. Y., VON HILDEBRAND, P., JIMÉNEZ, E., PATIÑO, S., PEÑUELA, M. C., PHILLIPS, O. L., STEVENSON, P. & MALHI, Y. 2010. Regional and seasonal patterns of litterfall in tropical South America. Biogeosciences 7:4355.Google Scholar
CLARK, D. A., BROWN, S., KICKLIGHTER, D. W., CHAMBERS, J. Q., THOMLINSON, J. R. & NI, J. 2001a. Measuring net primary production in forests: concepts and field methods. Ecological Applications 11:356370.Google Scholar
CLARK, D. A., BROWN, S., KICKLIGHTER, D. W., CHAMBERS, J. Q., THOMLINSON, J. R., NI, J. & HOLLAND, E. A. 2001b. Net primary production in tropical forests: an evaluation and synthesis of existing field data. Ecological Applications 11:371384.Google Scholar
CORDELL, S., GOLDSTEIN, G., MUELLER-DOMBOIS, D., WEBB, D. & VITOUSEK, P. M. 1998. Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity. Oecologia 113:188196.Google Scholar
CORDELL, S., GOLDSTEIN, G., MEINZER, F. C. & HANDLEY, L. L. 1999. Allocation of nitrogen and carbon in leaves of Metrosideros polymorpha regulates carboxylation capacity and δ13C along an altitudinal gradient. Functional Ecology 13:811818.Google Scholar
CORDERO, R. A. 1999. Ecophysiology of Cecropia schreberiana saplings in two wind regimes in an elfin cloud forest: growth, gas exchange, architecture and stem biomechanics. Tree Physiology 19:153163.Google Scholar
CRAVEN, D., HALL, J. S., ASHTON, M. A. & BERLYN, G. P. 2013. Water-use efficiency and whole-plant performance of nine tropical tree species at two sites with contrasting water availability in Panama. Trees 27:639653.Google Scholar
CUNNINGHAM, S. C. 2005. Photosynthetic responses to vapour pressure deficit in temperate and tropical evergreen rainforest trees of Australia. Oecologia 142:521528.Google Scholar
DARBY, A., DRAGULIC, D., GLUNK, A. & GOTSCH, S. G. 2016. Habitat moisture drives transpiration and foliar water uptake in a tropical montane cloud forest canopy. Oecologia in press. doi: 10.1007/s00442-016-3659-5.CrossRefGoogle Scholar
DAWSON, T. E. 1998. Fog in the California redwood forest: ecosystem inputs and use by plants. Oecologia 117:476485.Google Scholar
DAWSON, T. E., BURGESS, S. S. O., TU, K. P., RA, R. S., SANTIAGO, L. S., FISHER, J. B., SIMONIN, K. A. & AMBROSE, A. R. 2007. Nighttime transpiration in woody plants from contrasting ecosystems. Tree Physiology 27:561575.Google Scholar
DENGEL, S. & GRACE, J. 2010. Carbon dioxide exchange and canopy conductance of two coniferous forests under various sky conditions. Oecologia 164:797808.Google Scholar
ELLER, C. B., BURGESS, S. O. & OLIVEIRA, R. S. 2015. Environmental controls in water use patterns of a tropical cloud forest tree species, Drimys braciliensis (Winteraceae). Tree Physiology 35:387399.Google Scholar
FATICHI, S., LEUZINGER, S. & KÖRNER, C. 2014. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytologist 201:10861095.Google Scholar
FEILD, T. S. & HOLBROOK, N. M. 2000. Xylem sap flow and stem hydraulics of the vesselless angiosperm Drimys granadensis (Winteraceae) in a Costa Rican elfin forest. Plant Cell and Environment 23:10671077.Google Scholar
FERNÁNDEZ-MARTÍNEZ, M., VICCA, S., JANSSENS, I. A., LUYSSAERT, S., CAMPIOLI, M., SARDANS, J., ESTIARTE, M. & PEÑUELAS, J. 2014. Spatial variability and controls over biomass stocks, carbon fluxes, and resource-use efficiencies across forest ecosystems. Trees 28:597611.Google Scholar
FRANKS, P. J., ADAMS, M. A., AMTHOR, J. S., BARBOUR, M. M., BERRY, J. A., ELLSWORTH, D. S., FARQUHAR, G. D., GHANNOUM, O., LLOYD, J., MCDOWELL, N., NORBY, R. J., TISSUE, D. T. & VON CAEMMERER, S. 2013. Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytologist 197:10771094.Google Scholar
GALE, J. 1972. Availability of carbon dioxide for photosynthesis at high altitudes: theoretical considerations. Ecology 53:494497.Google Scholar
GIAMBELLUCA, T. W., MARTIN, R. E., ASNER, G. P., HUANG, M. Y. & MUDD, R. G. 2009. Evapotranspiration and energy balance of native wet montane cloud forest in Hawai'i. Agricultural and Forest Meteorology 149:230243.Google Scholar
GIRARDIN, C. A., ARAGÃO, L. E. O. C., MALHI, Y., HUARACA HUASCO, W., METCALFE, D. B., DURAND, L., MAMANI, M., SILVA-ESPEJO, J. E. & WHITTAKER, R. J. 2013. Fine root dynamics along an elevational gradient in tropical Amazonian and Andean forests. Global Biogeochemical Cycles 27:252264.Google Scholar
GIRARDIN, C. A. J., ESPEJOB, J. E. S., DOUGHTY, C. E., HUASCO, W. H., METCALFE, D. B., DURAND-BACA, L., MARTHEWS, T. R., ARAGÃO, L. E. O. C., FARFÁN-RIOS, W., GARCÍA-CABRERA, K., HALLADAY, K., FISHER, J. B., GALIANO-CABRERA, D. F., HUARACA-QUISPE, L. P., ALZAMORA-TAYPE, I., EGUILUZ-MORA, L., SALINAS-REVILLA, N., SILMAN, M. R., MEIR, P. & MALHI, Y. 2014. Productivity and carbon allocation in a tropical montane cloud forest in the Peruvian Andes. Plant Ecology and Diversity 7:107123.Google Scholar
GOLDSMITH, G. R., MATZKE, N. J. & DAWSON, T. E. 2013. The incidence and implications of clouds for cloud forest plant water relations. Ecology Letters 16:307314.Google Scholar
GOLDSTEIN, G., ANDRADE, F. C., MEINZER, F. C., HOLBROOK, N. M., CAVELIER, J., JACKSON, P. & CELIS, A. 1998. Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell and Environment 21:397406.Google Scholar
GÓMEZ-GUERRERO, A., SILVA, L. C. R., BARRERA-REYES, M., KISHCHUK, B., VELÁZQUEZ-MARTÍNEZ, A., MARTÍNEZ-TRINIDAD, T., PLASCENCIA-ESCALANTE, F. O. & HORWATH, W. R., 2013. Growth decline and divergent tree ring isotopic composition (δ13C and δ18O) contradict predictions of CO2 stimulation in high altitudinal forests. Global Change Biology 19:17481758.Google Scholar
GOTSCH, S. G., CRAUSBAY, C. S., GIAMBELLUCA, T. W., WEINTRAUB, A. E., LONGMAN, R. J., ASBJORNSEN, H., HOTCHKISS, S. C. & DAWSON, T. E. 2014a. Water relations and microclimate around the upper limit of a cloud forest in Maui, Hawai‘i. Tree Physiology 34:766777.Google Scholar
GOTSCH, S. G., ASBJORNSEN, H., HOLWERDA, F., GOLDSMITH, G. R., WEINTRAUB, A. E. & DAWSON, T. E. 2014b. Foggy days and dry nights determine crown-level water balance in a seasonal tropical montane cloud forest. Plant Cell and Environment 37:261272.Google Scholar
GOTSCH, S. G., NADKARNI, N., DARBY, A., GLUNK, A., DIX, M., DAVIDSON, K. & DAWSON, T. E. 2015. Life in the treetops: ecophysiological strategies of canopy epiphytes in a tropical montane cloud forest. Ecological Monographs 85:393412.Google Scholar
GRAHAM, E. A., MULKEY, S., KITAJIMA, K., NG, P. & WRIGHT, S. J. 2003. Cloud cover limits net CO2 uptake and growth of a rainforest tree during tropical rainy seasons. Proceedings of the National Academy of Sciences USA 100:572576.Google Scholar
GRUBB, P. J. 1971. Interpretation of the ‘Massenerhebung’ effect on tropical mountains. Nature 229:4445.Google Scholar
GRUBB, P. J. 1977. Control of forest growth and distribution on wet tropical mountains: with special reference to mineral nutrition. Annual Review of Ecology and Systematics 8:83107.Google Scholar
GU, L., BALDOCCHI, D., VERMA, S. B., BLACK, T. A., VESALA, T., FALGE, E. M. & DOWTY, P. R. 2002. Advantages of diffuse radiation for terrestrial ecosystem productivity. Journal of Geophysical Research 107 (D6):123.Google Scholar
GU, L., BALDOCCHI, D. D., WOFSY, S. C., MUNGER, J. W., MICHALSKY, J. J., URBANSKI, S. P. & BODEN, T. A. 2003. Response of a deciduous forest to the Mount Pinatubo eruption: enhanced photosynthesis. Science 299:20352038.Google Scholar
HAGER, A. & DOHRENBUSCH, A. 2011. Hydrometeorology and structure of tropical montane cloud forests under contrasting biophysical conditions in Northwestern Costa Rica. Hydrological Processes 25:392401.Google Scholar
HERWITZ, S. R. & YOUNG, S. S. 1994. Mortality, recruitment, and growth rates of montane tropical rain forest canopy trees on Mount Bellenden-Ker, Northeast Queensland, Australia. Biotropica 26:350361.Google Scholar
HIKOSAKA, K., NAGAMATSU, D., ISHII, H. S. & HIROSE, T. 2002. Photosynthesis–nitrogen relationships in species at different altitudes on Mount Kinabalu, Malaysia. Ecological Research 17:305313.Google Scholar
HOLDER, C. 2008. Diameter growth and decline in a tropical montane cloud forest of the Sierra de las Minas, Guatemala. Journal of Tropical Forest Science 20:292299.Google Scholar
HOLLINGER, D. Y., KELLIHER, F. M., BYERS, J. N., HUNT, J. E., MCSEVENY, T. M. & WEIR, P. L. 1994. Carbon dioxide exchange between an undisturbed old-growth temperate forest and the atmosphere. Ecology 75:134150.Google Scholar
HOLWERDA, F. 2005. Water and energy budgets of rain forests along an elevation gradient under maritime tropical conditions. Ph.D. dissertation, VU University Amsterdam, Amsterdam. 167 pp.Google Scholar
HOLWERDA, F., BRUIJNZEEL, L. A., MUÑOZ-VILLERS, L. E., EQUINA, M. & ASBJORNSEN, H. 2010. Rainfall and cloud water interception in mature and secondary lower montane cloud forests of central Veracruz, Mexico. Journal of Hydrology 384:8496.Google Scholar
HOMEIER, J., BRECKLE, S.-W., GÜNTER, S., ROLLENBECK, R. T. & LEUSCHNER, C. 2010. Tree diversity, forest structure and productivity along altitudinal and topographical gradients in a species-rich Ecuadorian montane rain forest. Biotropica 42:140148.Google Scholar
HUARACA HUASCO, W., GIRARDIN, C. A. J., DOUGHTY, C. E., METCALFE, D. B., BACA, L. D., SILVA-ESPEJO, J. E., CABRERA, D. G., ARAGÃO, L. E. O. C., DAVILA, A. R., MARTHEWS, T. R., HUARACA-QUISPE, L. P., ALZAMORA-TAYPE, I., MORA, L. E., FARFÁN-RIOS, W., CABRERA, K. G., HALLADAY, K., SALINAS-REVILLA, N., SILMAN, M. R., MEIR, P. & MALHI, Y. 2014. Seasonal production, allocation and cycling of carbon in two mid-elevation tropical montane forest plots in the Peruvian Andes. Plant Ecology and Diversity 7:118.Google Scholar
JARVIS, A. & MULLIGAN, M. 2011. The climate of cloud forests. Hydrological Processes 25:327343.Google Scholar
KITAYAMA, K. & AIBA, S. 2002. Ecosystem structure and productivity of tropical rain forest along altitudinal gradients with contrasting soil phosphorus pools on Mount Kinabalu, Borneo. Journal of Ecology 90:3751.Google Scholar
KARMALKAR, A. V., BRADLEY, R. S. & DIAZ, H. F. 2008. Climate change scenario for Costa Rican montane forests. Geophysical Research Letters 35:L11702.Google Scholar
KARMALKAR, A. V., BRADLEY, R. S. & DIAZ, H. F. 2011. Climate change in Central America and Mexico: regional climate model validation and climate change projections. Climate Dynamics 37:605629.Google Scholar
KÖRNER, C. 1999. Alpine plant life. (Second edition). Springer, Berlin. 345 pp.Google Scholar
KÖRNER, C. 2003. Carbon limitation in trees. Journal of Ecology 91:417.Google Scholar
LAW, B. E., FALGE, E., GU, L. V., BALDOCCHI, D. D., BAKWIN, P., BERBIGIER, P., DAVIS, K., DOLMAN, A. J., FALK, M. & FUENTES, J. D. 2002. Environmental controls over carbon dioxide and water vapor exchange of terrestrial vegetation. Agricultural and Forest Meteorology 113:97120.Google Scholar
LAWTON, R. O., NAIR, U. S., PIELKE, R. A. & WELCH, R. M. 2001. Climatic impact of tropical lowland deforestation on nearby montane cloud forests. Science 294: 584587.Google Scholar
LETTS, M. G. & MULLIGAN, M. 2005. The impact of light quality and leaf wetness on photosynthesis in north-west Andean tropical montane cloud forest. Journal of Tropical Ecology 21:549557.Google Scholar
LETTS, M. G., MULLIGAN, M., RINCÓN-ROMERO, M. E. & BRUIJNZEEL, L. A. 2010. Environmental controls on photosynthetic rates of lower montane cloud forest vegetation in south-western Colombia. Pp. 465478 in Bruijnzeel, L. A., Scatena, F. N. & Hamilton, L. S. (eds.). Tropical montane cloud forests: science for conservation and management. Cambridge University Press, Cambridge.Google Scholar
LEUSCHNER, C., MOSER, G., BERTSCH, C., RÖDERSTEIN, M. & HERTEL, D. 2007. Large altitudinal increase in tree root/shoot ratio in tropical mountain forests of Ecuador. Basic and Applied Ecology 8:219230.Google Scholar
LEUSCHNER, C., ZACH, A., MOSER, G., HOMEIER, J., GRAEFE, S., HERTEL, D., WITTICH, B., SOETHE, N., IOST, S., RÖDERSTEIN, M., HORNA, V. & WOLF, K. 2013. The carbon balance of tropical mountain forests along an altitudinal transect. Pp. 117139 in Bendix, J., Beck, E., Bräuning, A., Makeschin, F., Mosandl, R., Scheu, S. & Wilcke, W. (eds.). Ecosystem services, biodiversity and environmental change in a tropical mountain ecosystem of south Ecuador. Springer, Berlin.Google Scholar
LEVESQUE, M., SIEGWOLF, R., SAURER, M., EILMANN, B. & RIGLING, A. 2014. Increased water-use efficiency does not lead to enhanced tree growth under xeric and mesic conditions. New Phytologist 203:94109.Google Scholar
LLOYD, J. & FARQUHAR, G. D. 2008. Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philosophical Transactions of the Royal Society B: Biological Sciences 363:18111817.Google Scholar
LÜTTGE, U. 2007. Physiological ecology of tropical plants. (Second edition). Springer, Berlin. 456 pp.Google Scholar
MALHI, Y., AMÉZQUITA, F. F., DOUGHTY, C. E., SILVA-ESPEJO, J. E., GIRARDIN, C. A. J., METCALFE, D. B., ARAGÃO, L. E. O. C., HUARACA-QUISPE, L. P., ALZAMORA-TAYPE, I., EGUILUZ-MORA, L., MARTHEWS, T. R., HALLADAY, K., QUESADA, C. A., L, R. A., FISHER, J. B., ZARAGOZA-CASTELLS, J., ROJAS-VILLAGRA, C. M., PELAEZ-TAPIA, Y., SALINAS, N., MEIR, P. & PHILLIPS, O. L. 2014. The productivity, metabolism and carbon cycle of two lowland tropical forest plots in south-western Amazonia, Peru. Plant Ecology and Diversity 7:121.Google Scholar
MALHI, Y., DOUGHTY, C. E., GOLDSMITH, G. R., METCALFE, D. B., GIRARDIN, C. A. J., MARTHEWS, T. R., DEL AGUILA-PASQUEL, J., ARAGÃO, L. E. O. C., ARAUJO-MURAKMI, A., BRANDO, P., DA COSTA, A. C. L., SILVA-ESPEJO, J. E., FARFÁN AMÉZQUITA, F., GALBRAITH, D. R., QUESADA, C. A., ROCHA, W., SALINAS-REVILLA, N., SILVÉRIO, D., MEIR, P. & PHILLIPS, O. L. 2015. The linkages between photosynthesis, productivity, growth and biomass in lowland Amazonian forests. Global Change Biology 21:22832295.Google Scholar
MCJANNET, D. P., FITCH, P., DISHER, M. & WALLACE, J. 2007. Measurements of transpiration in four tropical rainforest types of north Queensland, Australia. Hydrological Processes 21:35493564.Google Scholar
MEINZER, F. C., GOLDSTEIN, G., HOLBROOK, N. M., JACKSON, P. & CAVELIER, J. 1993. Stomatal and environmental control of transpiration in a lowland tropical forest tree. Plant Cell and Environment 16:429436.Google Scholar
MEINZER, F. C., ANDRADE, J. L., GOLDSTEIN, G., HOLBROOK, N. M., CAVELIER, J. & JACKSON, P. 1997. Control of transpiration from the upper canopy of a tropical forest: the role of stomatal, boundary layer and hydraulic architecture components. Plant, Cell and Environment 20:12421252.Google Scholar
MOSER, G., LEUSCHNER, C., HERTEL, D., GRAEFE, S., SOETHE, N. & IOST, S. 2011. Elevation effects on the carbon budget of tropical mountain forests (S Ecuador): the role of the belowground compartment. Global Change Biology 17:22112226.Google Scholar
MOTZER, T., MUNZ, N., KUPPERS, M., SCHMITT, D. & ANHUF, D. 2005. Stomatal conductance, transpiration and sap flow of tropical montane rain forest trees in the southern Ecuadorian Andes. Tree Physiology 25:12831293.Google Scholar
MUÑOZ-VILLERS, L. E., HOLWERDA, F., GÓMEZ-CÁRDENAS, M., EQUIHUA, M., ASBJORNSEN, H., BRUIJNZEEL, L. A., MARÍN-CASTRO, B. E. & TOBÓN, C. 2012. Water balances of old-growth and regenerating montane cloud forests in central Veracruz, Mexico. Journal of Hydrology 462:5366.Google Scholar
NAGANO, S., TAKASHI, N., KOUKI, H., NAKANO, T., HIKOSAKA, K. & MARUTA, E. 2013. Pinus pumila photosynthesis is suppressed by water stress in a wind-exposed mountain site. Arctic Antarctic and Alpine Research 45:229237.Google Scholar
NEGRET, B. S., PEREZ, F., MARKESTEIJN, L., CASTILLO, M. J. & ARMESTO, J. J. 2013. Diverging drought-tolerance strategies explain tree species distribution along a fog-dependent moisture gradient in a temperate rain forest. Oecologia 173:625635.Google Scholar
NOGUEIRA, A., MARTINEZ, C. A., FERREIRA, L. L. & PRADO, C. H. B. A. 2004. Photosynthesis and water use efficiency in twenty tropical tree species of differing succession status in a Brazilian reforestation. Photosynthetica 42:351356.Google Scholar
OLIVEIRA, R. S., ELLER, C. B., BITTENCOURT, P. R. L. & MULLIGAN, M. 2014. The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates. Annals of Botany 113:909920.Google Scholar
PEÑUELAS, J. & AZCÓN-BIETO, J. 1992. Changes in leaf δ13C of herbarium plant species during the last 3 centuries of CO2 increase. Plant, Cell and Environment 15:485489.Google Scholar
PEÑUELAS, J., CANADELL, J. G. & OGAYA, R. 2011. Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Global Ecology and Biogeography 20:597608.Google Scholar
POUNDS, A., FOGDEN, M. P. L. & CAMPBELL, J. 1999. Biological responses to climate change on a tropical mountain. Nature 398:611615.Google Scholar
POUNDS, J. A., BUSTAMENTE, M. R., COLOMA, L. A., CONSUEGRA, J. A., FOGDEN, M. P. L., FOSTER, P. N., LA MARCA, E., MASTERS, K.L., MERINO-VITERI, A., PUSCHENDORF, R., RON, S. R., SÁNCHEZ-AZOFEIFA, G. A., STILL, C. J. & YOUNG, B. E. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161167.Google Scholar
RADA, F., GARCÍA-NÚÑEZ, C. & ATAROFF, M. 2009. Leaf gas exchange in canopy species of a Venezuelan cloud forest. Biotropica 41:659664.Google Scholar
RAICH, J. W., RUSSELL, A. E. & VITOUSEK, P. M. 1997. Primary productivity and ecosystem development along an elevational gradient on Mauna Loa, Hawai'i. Ecology 78:707721.Google Scholar
REINHARDT, K. & SMITH, W. K. 2008. Impacts of cloud immersion on microclimate, photosynthesis and water relations of Abies fraseri (Pursh.) Poiret in a temperate mountain cloud forest. Oecologia 158:229238.Google Scholar
RICHARDSON, A. D., DENNY, E. G., SICCAMA, T. G. & LEE, X. 2003. Evidence for a rising cloud ceiling in eastern North America. Journal of Climate 16:20932098.Google Scholar
SANTIAGO, L. S. & DAWSON, T. E. 2014. Light use efficiency of California redwood forest understory plants along a moisture gradient. Oecologia 174:351363.Google Scholar
SANTIAGO, L. S., GOLDSTEIN, G., MEINZER, F. C., FOWNES, J. H. & MUELLER-DOMBOIS, D. 2000. Transpiration and forest structure in relation to soil waterlogging in a Hawaiian montane cloud forest. Tree Physiology 20:673681.Google Scholar
SAURER, M., SPAHNI, R., FRANK, D. C., JOOS, F., LEUENBERGER, M., LOADER, N. J., MCCARROLL, D., GAGEN, M., POULTER, B. & SIEGWOLF, R. T. W. 2014. Spatial variability and temporal trends in water-use efficiency of European forests. Global Change Biology 20:37003712.Google Scholar
SHERMAN, R. E., FAHEY, T. J., MARTIN, P. H. & BATTLES, J. J. 2012. Patterns of growth, recruitment, mortality and biomass across an altitudinal gradient in a neotropical montane forest, Dominican Republic. Journal of Tropical Ecology 28:483495.Google Scholar
SLOT, M., WRIGHT, S. J. & KITAJIMA, K. 2013. Foliar respiration and its temperature sensitivity in trees and lianas: in situ measurements in the upper canopy of a tropical forest. Tree Physiology 33:505515.Google Scholar
SOBRADO, M. A. 2003. Hydraulic characteristics and leaf water use efficiency in trees from tropical montane habitats. Trees 17:400406.Google Scholar
STILL, C. J., FOSTER, P. N. & SCHNEIDER, H. 1999. Simulating the effects of climate change on tropical montane cloud forests. Nature 398:608610.Google Scholar
STILL, C. J., RILEY, W. J., BIRAUD, S. C., NOONE, D. C., BUENNING, N. H., RANDERSON, J. T., TORN, M. S., WELKER, J., WHITE, J. W. C., VACHON, R., FARQUHAR, G. D. & BERRY, J. A. 2009. Influence of clouds and diffuse radiation on ecosystem-atmosphere CO2 and CO18O exchanges. Journal of Geophysical Research 114:G01018.Google Scholar
TANAKA, K., TAKIZAWA, H., TANAKA, H., KOSAKA, I., YOSHIFUJI, N., TANTASIRIN, C., PIMAN, S., SUZUKI, M. & TANGTHAM, N. 2003. Transpiration peak over a hill evergreen forest in northern Thailand in the late dry season: assessing the seasonal changes in evapotranspiration using a multilayer model. Journal of Geophysical Research 108 (D17):4533.Google Scholar
TANAKA, N., KURAJI, K., TANTASIRIN, C., TAKIZAWA, H., TANGTHAM, N. & SUZUKI, M. 2011. Relationships between rainfall, fog and throughfall at a hill evergreen forest site in northern Thailand. Hydrological Processes 25:384391.Google Scholar
TANNER, E. V. J. 1980. Studies on the biomass and productivity in a series of montane rain forests in Jamaica. Journal of Ecology 68:573588.Google Scholar
URBAN, O., JANOUŠ, D., ACOSTA, M., CZERNÝ, R., MARKOVA, I., NAVRATIL, M., PAVELKA, M., POKORNÝ, R., ŠPRTOVÁ, M. & ZHANG, R. 2007. Ecophysiological controls over the net ecosystem exchange of mountain spruce stand. Comparison of the response in direct vs. diffuse solar radiation. Global Change Biology 13:157168.Google Scholar
URBAN, O., KLEM, K., , A., HAVRÁNKOVÁ, K., HOLIŠOVÁ, P., NAVRATIL, M., ZITOVÁ, M., KOZLOVÁ, K., POKORNÝ, R., ŠPRTOVÁ, M., TOMÁŠKOVÁ, I., ŠPUNDA, V. & GRACE, J. 2012. Impact of clear and cloudy sky conditions on the vertical distribution of photosynthetic CO2 uptake within a spruce canopy. Functional Ecology 26:4655.CrossRefGoogle Scholar
URRUTIA, R. & VUILLE, M. 2009. Climate change projections for the tropical Andes using a regional climate model: temperature and precipitation simulations for the end of the 21st century. Journal of Geophysical Research 114:D02108.Google Scholar
VAN DE WEG, M. J., MEIR, P., GRACE, J. & ATKIN, O. K. 2009. Altitudinal variation in leaf mass per unit area, leaf tissue density and foliar nitrogen and phosphorus content along an Amazon-Andes gradient in Peru. Plant Ecology and Diversity 2:243254.Google Scholar
VAN DE WEG, M. J., MEIR, P., GRACE, J. & RAMOS, G. D. 2012. Photosynthetic parameters, dark respiration and leaf traits in the canopy of a Peruvian tropical montane cloud forest. Oecologia 168:2334.Google Scholar
VAN DER SLEEN, P., GROENENDIJK, P., VLAM, M., ANTEN, N. P. R., BOOM, A., BONGERS, F., PONS, T. L., TERBURG, G. & ZUIDEMA, P. A. 2015. No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nature Geoscience 8:2428.Google Scholar
VANDERWEL, M. C., SLOT, M., LICHTSTEIN, J. W., REICH, P. B., KATTGE, J., ATKIN, O. K., BLOOMFIELD, K. J., TJOELKER, M. G. & KITAJIMA, K. 2015. Global convergence in leaf respiration from estimates of thermal acclimation across time and space. New Phytologist 207:10261037.Google Scholar
VARGAS, G. G. & CORDERO, R. A. 2013. Photosynthetic responses to temperature of two tropical rainforest tree species from Costa Rica. Trees – Structure and Function 27:12611270.Google Scholar
VASEY, M. C., LOIK, M. E. & PARKER, T. V. 2012. Influence of summer marine fog and low cloud stratus on water relations of evergreen woody shrubs (Arctostaphylos: Ericaceae) in the chaparral of central California. Oecologia 170:325337.Google Scholar
WANG, H., HALL, C. A. S., SCATENA, F. N., FETCHER, N. & WU, W. 2003. Modeling the spatial and temporal variability in climate and productivity across the Luquillo Mountains, Puerto Rico. Forest Ecology and Management 179:6994.Google Scholar
WEAVER, P. L. & MURPHY, P. G. 1990. Forest structure and productivity in Puerto Rico's Luquillo Mountains. Biotropica 22:6982.Google Scholar
WEAVER, P. L., MEDINA, E., POOL, D., DUGGER, K., GONZALES-LIBOY, J. & CUEVAS, E. 1986. Ecological observations in the dwarf cloud forest of the Luquillo Mountains in Puerto Rico. Biotropica 18:7985.Google Scholar
WHITMORE, T. C. 1998. An introduction to tropical rain forests. Oxford University Press, Oxford. 296 pp.Google Scholar
WILLIAMS, J. W., JACKSON, S. T. & KUTZBACH, J. E. 2007. Projected distributions of novel and disappearing climates by 2100 AD. Proceedings of the National Academy of Sciences USA 104:57385742.Google Scholar
WITTICH, B., HORNA, V., HOMEIER, J. & LEUSCHNER, C. 2012. Altitudinal change in the photosynthetic capacity of tropical trees: a case study from Ecuador and a pantropical literature analysis. Ecosystems 15:958973.Google Scholar
WÜRTH, M. K. R., PELÁEZ-RIEDL, S., WRIGHT, S. J. & KÖRNER, C. 2005. Non-structural carbohydrate pools in a tropical forest. Oecologia 143:1124.Google Scholar
ZOTZ, G., TYREE, M. T., PATINO, S. & CARLTON, M. R. 1998. Hydraulic architecture and water use of selected species from a lower montane forest in Panama. Trees – Structure and Function 12:302309.Google Scholar