The seasonal climate drivers of the carbon cycle in tropical forests remain
poorly known, although these forests account for more carbon assimilation and
storage than any other terrestrial ecosystem. Based on a unique combination
of seasonal pan-tropical data sets from 89 experimental sites (68 include
aboveground wood productivity measurements and 35 litter productivity
measurements), their associated canopy photosynthetic capacity (enhanced
vegetation index, EVI) and climate, we ask how carbon assimilation and
aboveground allocation are related to climate seasonality in tropical forests
and how they interact in the seasonal carbon cycle. We found that canopy
photosynthetic capacity seasonality responds positively to precipitation when
rainfall is
Tropical forests have a primary role in the terrestrial carbon (C) cycle.
They constitute 54 % of the total aboveground biomass carbon of Earth's
forests
Despite long-term investigation of changes in forest aboveground biomass
stock and carbon fluxes, the direct effect of climate on the seasonal carbon
cycle of tropical forests remains unclear. Contrasting results have been
reported depending on methods used. Studies show an increase of aboveground
biomass gain in the wet season from direct measurement (biological field
measurements), or, from indirect measurement, an increase of canopy
photosynthetic capacity in the dry season (remote sensing, flux tower
network)
Here, we determine the dependence of seasonal aboveground wood productivity,
litterfall and canopy photosynthetic capacity (using the MODIS enhanced
vegetation index (EVI) as a proxy) on climate across the tropics, and assess
their interconnections in the seasonal carbon cycle. EVI strongly correlated
with chlorophyll content and photosynthetic activity
Geographical locations of the 89 observation sites with the field
measurement types (wood productivity and/or litter productivity) and global
ecological zones
We compiled publications reporting seasonal wood productivity of tropical
forests. Seasonal tree growth measurements in 68 pantropical forest sites,
representing 14 481 individuals, were obtained from published sources or
directly from the authors (Table
Description of the study sites. For each site, continent (cont.)
(Africa – Af, America – Am, Asia – As and Australia – Aus), country, full
site name and geographical coordinates (long.-lat., in decimal degrees) are
reported. The next column reports the site's type of measurements: wood
productivity and litterfall (WP
Continued.
Seasonal litterfall productivity measurements from a previously published
meta-analysis were used for South America
Enhanced vegetation index (EVI) was used as a proxy for canopy photosynthetic
capacity in tropical forest regions
Description of the study sites for litterfall measurements,adapted
from
To extract the monthly climate time series for the 89 experimental sites
(Fig.
Because at some sites wood productivity or litterfall measurements are older than the EVI measurements (before 2002), and, for recent site measurements, climate data are not yet available (after 2012), all the data sets were averaged monthly by site. Then, in order to remove the site effect on the mean and the variance of the variables and to analyse only seasonality, all the variables were centred on zero and scaled to a variance of 1 by site. That is, for a given variable of a site, monthly values were subtracted by their annual mean and divided by their annual standard deviation. The obtained normalized variable had a mean of 0 and a variance of 1, but the time variation in the variable time-series, that is in our case the seasonality, remained completely unchanged.
The 89 sites represent a large sample of tropical forests under different
tropical and subtropical climates corresponding to six global ecological
tropical zones
Changes in tree circumference measured with dendrometers are commonly used to
characterise seasonal wood productivity. However, accelerated changes in
circumference increments during the onset of the wet season can be caused by
bark swelling as stems become hydrated
In a temperate forest,
Coefficient of the linear model of wood productivity with
the precipitation; with all data
To address the first question “Are seasonal aboveground wood productivity,
litterfall productivity and photosynthetic capacity dependent on climate?”,
we analysed with linear models the relationship between our variable of
interest (wood productivity, litterfall productivity and photosynthetic
capacity) and each climate variable at each site and at
When the climate variable with direct effect was identified, we built a
linear model to predict wood and litter productivity seasonality with climate
in all sites. For EVI, two climate variables were identified and their
influence was dependent on the site values of
To address the second question “Does a coherent pan-tropical rhythm exist among these three key components of the forest carbon fluxes?”, we analysed the linear relationship between wood, litter productivity and canopy photosynthetic capacity. The non-parametric Mann-Whitney test was used to determine the association between wood/litter productivity and photosynthesis rhythmicity depending on site limitations.
To address the third question – is the rhythm among these three key
components of the forest carbon controlled by exogenous (climate) or
endogenous (ecosystem) processes? – we analysed the linear relationship
between
To avoid over-representation of sites with the “same climate” (that is, to account for spatial and temporal autocorrelation in the climate data) cross correlation (positive and negative) were computed within sites for the monthly climate variables rad, pre, pet, dtr, tmn and tmx. The site's annual values of the same climate variables were added in the table. After scaling and centring the table, the Euclidian distance between each site and the mean table of all other sites (barycentre) was computed. We defined the weight of each site as the distance to the other divided by the maximum distance to the other. This distance was used as a weight in the linear models.
All analysis were performed in
A direct and dominant signal of precipitation seasonality was found in
seasonality of wood productivity for 59 out of the 68 sites (86.8 %) where
wood productivity data were available (cluster of variables in Fig. 2a with
temperature amplitude (dtr), cloud cover (cld), precipitation (pre) and soil
water content (swc), Sect. 2.2 and Supplement Table S1). All the variables in
this cluster are wet season indicators: low temperature amplitude, high
precipitation, high soil water content and high cloud cover. Two other
clusters of climate variables are apparently associated with wood
productivity. However, the climate variables that better explained wood
productivity in these two clusters, vapour pressure (vap) and mean
temperature (tmp), respectively, are highly correlated with precipitation in
the clusters (Fig.
Dendrogram of the climate seasonality associations with the
seasonality of wood productivity
It is interesting to note that 48.0 % of the monthly wood productivity is
explained by the single variable “precipitation” (model
Intercepts and slopes of the fitted linear models for seasonal wood
production (
Observed vs. predicted monthly wood productivity under the model
only with precipitation,
Cross correlation between observations and predictions of wood
production
Monthly associations of EVI with precipitation
Threshold of
Locations and climate limitations of the 89 experimental sites.
water-limited sites (
Association between normalized maximal temperature from Climate
Research Unit and normalized incoming solar radiation at the surface from
CERES. Monthly incoming solar radiation at the surface (incident shortwave
radiation) refers to radiant energy with wavelengths in the visible,
near-ultraviolet, and near-infrared spectra and is produced using MODIS data
and geostationary satellite cloud properties
Observations and predictions of wood productivity and litterfall
seasonality in sites where both measurements were available. The outliers in
our analysis, Lambir and Caracarai, are not represented.
Cross-correlation between monthly EVI and wood productivity
Canopy photosynthetic capacity, as estimated by EVI, for the 89 experimental
sites, displayed an intriguing pattern with monthly precipitation, apparently
related to the difference of
For 27 out of the 35 sites (77.1 %) where litter data were available,
litter productivity was associated with dry season indicators (lack of
precipitation, high evaporation, low soil water content and high temperature
amplitude, Fig.
At a pan-tropical scale, 48 % of the variability of monthly aboveground
wood productivity (Fig.
In sites where both measurements were available, we observed a negative
relationship between wood productivity and litterfall (Fig.
In water-limited forests, the seasonality EVI and aboveground wood production
are synchronous for the majority of the sites (Fig.
Conversely, in light-limited sites and forests with mixed limitations (mixed
forests), EVI is weakly coupled with the seasonality of wood productivity
(respectively
The relationship between EVI and litter production is not constant
(Fig.
Associations between site's
We have found a remarkably strong climate signal in the seasonal carbon cycle components studied across tropical forests. While wood and litterfall production appear to be dependent on a single major climate driver across the tropics (water availability), the control of photosynthetic capacity varies according to the increase in annual water availability, shifting from water-only to light-only drivers.
Minimum aboveground wood production tends to occur in the dry season. While
this result is not new
Maximum litterfall, for most of our sites, occurs during the months of
minimum cloud cover during the dry season. It is known that the gradient from
deciduous to evergreen forests is related to water availability, with the
evergreen state sustained during the dry season above a mean annual
precipitation threshold of approximately 2000 mm yr
Canopy photosynthetic capacity has different climate controls depending on
water limitations (Fig.
We demonstrated that the seasonality of aboveground wood production and
litterfall are coupled, while photosynthetic capacity seasonality can be
decoupled from wood and litterfall production seasonality depending on the
local water availability (Fig.
Further, our results show that carbon allocation to wood is prioritized in
the wet season, independently of the site conditions (water- or
light-limited). This priority has also been shown in forests impacted by
droughts, where trees prioritised wood production by reducing autotrophic
respiration even when photosynthesis was reduced as a consequence of water
shortage
Canopy photosynthetic capacity and aboveground wood production appear to be
predominantly driven by climate at seasonal and annual scales, thereby
suggesting exogenous drivers (Figs.
In this study, we use EVI as an index of seasonality of canopy photosynthetic
capacity based on the previously demonstrated correlation between canopy
photosynthetic capacity from the MODIS sensor and solar-induced chlorophyll
fluorescence (SIF) at a pan-tropical scale
In summary, the seasonality of carbon assimilation and allocation through photosynthetic capacity and aboveground wood production is consistently and directly related to climate in tropical forested regions. Notably, we found that regions without annual water limitations exhibit a decoupled carbon assimilation and storage cycle, which highlight the complexity of carbon allocation seasonality in the tropical trees. Although seasonal carbon allocation to aboveground wood production is driven by water, whether the seasonality of photosynthetic capacity is driven by light or water depends on the limitations of site water availability.
In a drier climate, from our results we can make the following assumptions.
(i) In water-limited forests, the reduction of the wet period duration could
lead to a time reduction of favourable conditions for carbon assimilation and
allocation. (ii) In current light-limited forests with future precipitation
below to the 2000 mm yr
Despite this dominant signal, outliers exist in our data showing negative (3
sites) or no relationship (6 sites) with precipitation. Due to the
correlation of climate variables at the site scale, it is difficult to
interpret each site alone; however, some groups arose in these outlier sites.
The first group, the two sites Itatinga and Pinkwae, contains only saplings
measurements. The second group, the sites with no month with precipitation
below 100 mm, includes Lambir (Malaysia), Muara Bungo (Indonesia), Pasoh
(Malaysia), Flona SFP (Brazil). The third group includes two mountain sites,
Tulua and Munessa. For Munessa, there is evidence of cambial growth related
to precipitation
Only one site, BDFFP, showed no apparent relationship between litter
productivity and cloud cover (Fig. S3). This site is in a fragmented forest
where fragmentation is known to affect litterfall
The data and the code to reproduce the analysis and the figures are freely available upon request to the corresponding author.
Fabien H. Wagner, Luiz E. O. C. Aragão, Bruno Hérault, Damien Bonal and Clément Stahl wrote the paper, Fabien H. Wagner, Luiz E. O. C. Aragão and Bruno Hérault conceived and designed the study, Fabien H. Wagner assembled the data sets, Benjamin Brede and Jan Verbesselt contributed to the programming part, Fabien H. Wagner carried out the data analysis. All co-authors collected field data and commented on or approved the manuscript.
This project and F. H. W. have been funded by the Fapesp (Fundação de Amparo à Pesquisa do Estado de São Paulo, processo 13/14520-6). L. E. O. C. A. thank the support of FAPESP (grant 50533-5) and CNPQ (grant 304425/2013-3). J. P. L. and M. M. T. were funded by the CNPq and the FAPEMIG. B. P. M. was funded by the Australian Research Council for the project “Understanding the impact of global environmental change on Australian forests and woodlands using rainforest boundaries and Callitris growth as bio-indicators”, grant number: DP0878177. A. B. was funded by the German Research Foundation (DFG) for the project BR1895/15 and the projects BR1895/14 and BR1895/23 (PAK 823). F. A. C. and J. M. F. were funded by the CNPq (grant 476477/2006-9) and the Fundação O Boticário de Proteção a Natureza (grant 0705-2006). F. R. C. C. was funded by the CNPq/PELD “Impactos antrópicos no ecossistema de floresta tropical – site Manaus”, Processo 403764/2012-2. J. G. was supported from the US Forest Service-International Institute of Tropical Forestry. A. D. G. funding was provided through ARC Linkage (Timber harvest management for the Aboriginal arts industry: socio-economic, cultural and ecological determinants of sustainability in a remote community context, LP0219425). S. F. O. was funded by the National Science Foundation BE/CBC: Complex interactions among water, nutrients and carbon stocks and fluxes across a natural fertility gradient in tropical rain forest (EAR 421178) and National Science Foundation Causes and implications of dry season control of tropical wet forest tree growth at very high water levels: direct vs. indirect limitations (DEB 842235). E. E. M. was funded by the Academy of Finland (project: 266393). L. M. was funded by a grant provided by the European Union (FP6, INCO/SSA) for a 2 year (2006–2008) project on management of indigenous tree species for restoration and wood production in semi-arid miombo woodlands in East Africa (MITMIOMBO). F. V. was supported by the German Research Foundation (DFG) by funding the projects BR 1895/14-1/2 (FOR 816) and BR 1895/23-1/2 (PAK 823). L. K. K. was supported by the Malaysian Palm Oil Board. D. M. D. was funded by the Hermon Slade Foundation (Grant HSF 09/5). Data recorded at Paracou, French Guiana, were partly funded by an “Investissement d'Avenir” grant from the ANR (CEBA: ANR-10-LABX-0025). H. A. M. and J. J. C. thank the staff of the Jardín Botânico “Juan María Céspedes” (INCIVA, Colombia) and the Instituto Boliviano de Investigación Forestal (IBIF, Bolivia) for their support, particularly to M. Toledo and W. Devia; and P. Roosenboom (INPA Co.) and his staff at Concepción (G. Urbano) for their help in Bolivia. H. A. M. and J. J. C. were funded by the following research projects “Análisis retrospectivos mediante dendrocronología para profundizar en la ecología y mejorar la gestión de los bosques tropicales secos” (financed by Fundación BBVA) and “Regeneración, crecimiento y modelos dinámicos de bosques tropicales secos: herramientas para su conservación y para el uso sostenible de especies maderables” (AECID 11-CAP2-1730, Spanish Ministry of Foreign Affairs). C. S. L. was funded by a grant from FAPESP (Proc. 02/ 14166-3), and Brazilian Council for Superior Education, CAPES. J. H. was funded by two grants from the Deutsche Forschungsgemeinschaft (DFG): BR379/16 and HO3296/4. D. A. C. was funded by the US National Science Foundation (most recently EAR0421178 & DEB-1357112), the US Department of Energy, the Andrew W. Mellon Foundation, and Conservation International's TEAM Initiative. C. S. was funded by a grant from the “European Research 991 Council Synergy”, grant ERC-2013-SyG-610028 IMBALANCE-P. M. R. K., J. E. F. M., T. L. S. and F. G. were funded by Petrobras SA. We further thank Jeanine Maria Felfili and Raimundo dos Santos Saraiva who contributed to this work but who are no longer with us. Edited by: S. Zaehle