Abstract
For decades, the productivity of tropical montane cloud forests (TMCF) has been assumed to be lower than in tropical lowland forests due to nutrient limitation, lower temperatures, and frequent cloud immersion, although actual estimates of gross primary productivity (GPP) are very scarce. Here, we present the results of a process-based modeling estimate of GPP, using a soil–plant–atmosphere model, of a high elevation Peruvian TMCF. The model was parameterized with field-measured physiological and structural vegetation variables, and driven with meteorological data from the site. Modeled transpiration corroborated well with measured sap flow, and simulated GPP added up to 16.2 ± SE 1.6 Mg C ha−1 y−1. Dry season GPP was significantly lower than wet season GPP, although this difference was 17% and not caused by drought stress. The strongest environmental controls on simulated GPP were variation of photosynthetic active radiation and air temperature (T air). Their relative importance likely varies with elevation and the local prevalence of cloud cover. Photosynthetic parameters (V cmax and J max) and leaf area index were the most important non-environmental controls on GPP. We additionally compared the modeled results with a recent estimate of GPP of the same Peruvian TMCF derived by the summing of ecosystem respiration and net productivity terms, which added up to 26 Mg C ha−1 y−1. Despite the uncertainties in modeling GPP we conclude that at this altitude GPP is, conservatively estimated, 30–40% lower than in lowland rainforest and this difference is driven mostly by cooler temperatures than changes in other parameters.
Similar content being viewed by others
References
Adamek M, Corre MD, Holscher D. 2009. Early effect of elevated nitrogen input on above-ground net primary production of a lower montane rain forest, Panama. J Trop Ecol 25:637–47.
Bruijnzeel LA, Veneklaas EJ. 1998. Climatic conditions and tropical, montane forest productivity: the fog has not lifted yet. Ecology 79:3–9.
Čermák J, Deml M, Penka M. 1973. A new method of sap flow rate determination in trees. Biol Plant 15:171–8.
Čermák J, Kucera J, Nadezhdina N. 2004. Sap flow measurements with some thermodynamic methods, flow integration within trees and scaling up from sample trees to entire forest stands. Trees Struct Funct 18:529–46.
Domingues TF, Berry JA, Martinelli LA, Ometto J, Ehleringer JR. 2005. Parameterization of canopy structure and leaf-level gas exchange for an eastern Amazonian tropical rain forest (Tapajos National Forest, Para, Brazil). Earth Interact 9(17):1–23.
Farquhar GD, Caemmerer SV, Berry JA. 1980. A biochemical-model of photosynthetic CO2 assimilation in leaves of C-3 species. Planta 149:78–90.
Fisher JB, Malhi Y, Torres IC, Metcalfe DB, van de Weg MJ, Meir P, Silva-Espejo JE, Huasco WH. 2013. Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes. Oecologia 172(3):889–902.
Fisher JB, Malhi Y, Bonal D, Da Rocha HR, De AraÚJo AC, Gamo M, Goulden ML, Hirano T, Huete AR, Kondo H, Kumagai TO, Loescher HW, Miller S, Nobre AD, Nouvellon Y, Oberbauer SF, Panuthai S, Roupsard O, Saleska S, Tanaka K, Tanaka N, Tu KP, Von Randow C. 2009. The land–atmosphere water flux in the tropics. Glob Change Biol 15:2694–714.
Fisher RA, Williams M, da Costa AL, Malhi Y, da Costa RF, Almeida S, Meir P. 2007. The response of an eastern amazonian rain forest to drought stress: results and modelling analyses from a throughfall exclusion experiment. Glob Change Biol 13:2361–78.
Fisher RA, Williams M, de Lourdes Ruivo M, de Costa AL, Meir P. 2008. Evaluating climatic and soil water controls on evapotranspiration at two amazonian rainforest sites. Agric For Meteorol 148:850–61.
Fisher RA, Williams M, Do Vale RL, Da Costa AL, Meir P. 2006. Evidence from amazonian forests is consistent with isohydric control of leaf water potential. Plant Cell Environ 29:151–65.
Fox A, Williams M, Richardson AD, Cameron D, Gove JH, Quaife T, Ricciuto D, Reichstein M, Tomelleri E, Trudinger CM, Van Wijk MT. 2009. The REFLEX project: Comparing different algorithms and implementations for the inversion of a terrestrial ecosystem model against eddy covariance data. Agric For Meteorol 149(10):1597–615.
Girardin CAJ, Malhi Y, AragÃO LEOC, Mamani M, Huaraca Huasco W, Durand L, Feeley KJ, Rapp J, Silva-Espejo JE, Silman M, Salinas N, Whittaker RJ. 2010. Net primary productivity allocation and cycling of carbon along a tropical forest elevational transect in the Peruvian Andes. Glob Change Biol 16:3176–92.
Girardin CAJ et al. 2013. Productivity and carbon allocation in a tropical montane cloud forest in the Peruvian Andes. Plant Ecol Divers 7(1–2):55–69.
Grubb PJ, Whitmore TC. 1966. A comparison of montane and lowland rain forest in Ecuador. II. Climate and its effects on distribution and physiognomy of forests. J Ecol 54:303–33.
Hirata R, Saigusa N, Yamamoto S, Ohtani Y, Ide R, Asanuma J, Gamo M, Hirano T, Kondo H, Kosugi Y, Li S-G, Nakai Y, Takagi K, Tani M, Wang H. 2008. Spatial distribution of carbon balance in forest ecosystems across East Asia. Agric For Meteorol 148:761–75.
Hutyra LR, Munger JW, Hammond-Pyle E, Saleska SR, Restrepo-Coupe N, Daube BC, de Camargo PB, Wofsy SC. 2008. Resolving systematic errors in estimates of net ecosystem exchange of CO2 and ecosystem respiration in a tropical forest biome. Agric For Meteorol 148:1266–79.
Kaimal JC, Finnigan JJ. 1994. Atmospheric boundary layer flows: their structure and measurement. Oxford: Oxford University Press.
Kitayama K, Aiba SI. 2002. Ecosystem structure and productivity of tropical rain forests along altitudinal gradients with contrasting soil phosphorus pools on Mount Kinabalu, Borneo. J Ecol 90:37–51.
Lemmon PE. 1956. A spherical densiometer for estimating forest overstory density. For Sci 2:314–20.
Letts MG, Mulligan M. 2005. The impact of light quality and leaf wetness on photosynthesis in north-west Andean tropical montane cloud forest. J Trop Ecol 21:549–57.
Malhi Y, Aragao L, Metcalfe DB, Paiva R, Quesada CA, Almeida S, Anderson L, Brando P, Chambers JQ, da Costa ACL, Hutyra LR, Oliveira P, Patino S, Pyle EH, Robertson AL, Teixeira LM. 2009. Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Glob Change Biol 15:1255–74.
Marthews TR, Malhi Y, Girardin CAJ, Silva Espejo JE, Aragão LEOC, Metcalfe DB, Rapp JM, Mercado LM, Fisher RA, Galbraith DR, Fisher JB, Salinas-Revilla N, Friend AD, Restrepo-Coupe N, Williams RJ. 2012. Simulating forest productivity along a neotropical elevational transect: temperature variation and carbon use efficiency. Glob Change Biol 18:2882–98.
McMurtrie RE, Comins HN, Kirschbaum MUF, Wang YP. 1992. Modifying existing forest growth models to take account of effects of elevated CO2. Aust J Bot 40:657–77.
Meir P, Kruijt B, Broadmeadow M, Kull O, Carswell F, Nobre A, Jarvis PG. 2002. Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant Cell Environ 25:343–57.
Miller SD, Goulden ML, Menton MC, da Rocha HR, de Freitas HC, e Silva Figueira AM, Dias de Sousa CA. 2004. Biometric and micrometeorologicla measurements of tropical forest carbon balance. Ecol Appl 14(Suppl. 4):114–26.
Moser G, Hertel D, Leuschner C. 2007. Altitudinal change in Lai and stand leaf biomass in tropical montane forests: a transect shady in Ecuador and a pan-tropical meta-analysis. Ecosystems 10:924–35.
Raich JW, Russell AE, Vitousek PM. 1997. Primary productivity and ecosystem development along an elevational gradient on Mauna Loa, Hawaii. Ecology 78:707–21.
Robertson AL, Malhi Y, Farfan-Amezquita F, Aragão LEOC, Silva Espejo JE, Robertson MA. 2010. Stem respiration in tropical forests along an elevation gradient in the Amazon and Andes. Glob Change Biol 16(12):3193–204.
Ryan MG, Binkley D, Fownes JH, Giardina CP, Senock RS. 2004. An experimental test of the causes of forest growth decline with stand age. Ecol. Monogr 74(3):393–414.
Santiago LS, Goldstein G, Meinzer FC, Fownes JH, Mueller-Dombois D. 2000. Transpiration and forest structure in relation to soil waterlogging in a Hawaiian montane cloud forest. Tree Physiol 20:673–81.
Saxton KE, Rawls WJ, Romberger JS, Papendick RI. 1986. Estimating generalized soil-water characteristics from texture. Soil Sci Soc Am J 50:1031–6.
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL. 2007. Fitting photosynthetic carbon dioxide response curves for C-3 leaves. Plant Cell Environ 30:1035–40.
Tanner EVJ, Kapos V, Franco W. 1992. Nitrogen and phosphorus fertilization effects on Venezuelan montane forest trunk growth and litterfall. Ecology 73:78–86.
Tanner EVJ, Kapos V, Freskos S, Healey JR, Theobald AM. 1990. Nitrogen and phosphorus fertilization of Jamaican montane forest trees. J Trop Ecol 6:231–8.
Tanner EVJ, Vitousek PM, Cuevas E. 1998. Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22.
Tjoelker MG, Oleksyn J, Reich PB. 2001. Modelling respiration of vegetation: evidence for a general temperature-dependent Q10. Glob Change Biol 7(2):223–30.
van de Weg MJ, Meir P, Grace J, Atkin OK. 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 Ecol Divers 2:243–54.
van de Weg MJ, Meir P, Grace J, Damian Ramos G. 2012. Photosynthetic parameters, dark respiration and leaf traits in the canopy of a Peruvian tropical montane cloud forest. Oecologia 168:23–34.
Vitousek P, Farrington H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75.
Waide RB, Zimmerman JK, Scatena FN. 1998. Controls of primary productivity: lessons from the Luquillo Mountains in Puerto Rico. Ecology 79:31–7.
Wang HQ, Hall CAS, Scatena FN, Fetcher N, Wu W. 2003. Modeling the spatial and temporal variability in climate and primary productivity across the Luquillo Mountains, Puerto Rico. For Ecol Manage 179:69–94.
Williams M, Law BE, Anthoni PM, Unsworth MH. 2001a. Use of a simulation model and ecosystem flux data to examine carbon–water interactions in ponderosa pine. Tree Physiol 21(5):287–98.
Williams M, Malhi Y, Nobre AD, Rastetter EB, Grace J, Pereira MGP. 1998. Seasonal variation in net carbon exchange and evapotranspiration in a Brazilian rain forest: a modelling analysis. Plant Cell Environ 21:953–68.
Williams M, Rastetter EB, Fernandes DN, Goulden ML, Wofsy SC, Shaver GR, Melillo JM, Munger JW, Fan SM, Nadelhoffer KJ. 1996. Modelling the soil-plant-atmosphere continuum in a Quercus–Acer stand at Harvard Forest: the regulation of stomatal conductance by light, nitrogen and soil/plant hydraulic properties. Plant Cell Environ 19:911–27.
Williams M, Rastetter EB, Shaver GR, Hobbie JE, Carpino E, Kwiatkowski BL. 2001b. Primary production of an arctic watershed: an uncertainty analysis. Ecol Appl 11:1800–16.
Wright JK, Williams M, Starr G, McGee J, Mitchell RJ. 2013. Measured and modelled leaf and stand-scale productivity across a soil moisture gradient and a severe drought. Plant Cell Environ 36:467–83.
Wullschleger SD. 1993. Biochemical limitations to carbon assimilation in C3 plants: a retrospective analysis of the A/C i curves from 109 species. J Exp Bot 44:907–20.
Zimmermann M, Meir P, Bird MI, Malhi Y, Ccahuana AJQ. 2009. Climate dependence of heterotrophic soil respiration from a soil-translocation experiment along a 3000 m tropical forest altitudinal gradient. Eur J Soil Sci 60:895–906.
Zotz G, Tyree MT, Patino S, Carlton MR. 1998. Hydraulic architecture and water use of selected species from a lower montane forest in Panama. Trees Struct Funct 12:302–9.
Acknowledgments
This study is a product of the Andes Biodiversity and Ecosystems Research Group. This study was financed by a grant from the Andes-Amazon program of the Gordon and Betty Moore Foundation, with research grants from the UK Natural Environment Research Council, a Royal Geographical Society (with IBG) geographical fieldwork grant and a scholarship from the School of Geosciences from the University of Edinburgh. We also thank the Asociación para la Conservación de la Cuenca Amazónica (ACCA) for hosting us at the Wayqecha field station and INRENA for permitting us to explore the Peruvian tropical forest. We thank Rob St John for indispensible help with the sap flow system.
Author information
Authors and Affiliations
Corresponding author
Additional information
Author’s Contribution
PM, JG, and MvdW conceived of the study, MvdW, CG, and JS-E conducted the fieldwork, MvdW and CG analyzed the field work data, JS-E and YM provided additional field data, MW contributed the model, MvdW analyzed the model outcomes and all authors contributed to the manuscript.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
van de Weg, M.J., Meir, P., Williams, M. et al. Gross Primary Productivity of a High Elevation Tropical Montane Cloud Forest. Ecosystems 17, 751–764 (2014). https://doi.org/10.1007/s10021-014-9758-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-014-9758-4