In evergreen tropical forests, the extent, magnitude, and controls on photosynthetic seasonality are poorly resolved and inadequately represented in Earth system models. Combining camera observations with ecosystem carbon dioxide fluxes at forests across rainfall gradients in Amazônia, we show that aggregate canopy phenology, not seasonality of climate drivers, is the primary cause of photosynthetic seasonality in these forests. Specifically, synchronization of new leaf growth with dry season litterfall shifts canopy composition toward younger, more light-use efficient leaves, explaining large seasonal increases (~27%) in ecosystem photosynthesis. Coordinated leaf development and demography thus reconcile seemingly disparate observations at different scales and indicate that accounting for leaf-level phenology is critical for accurately simulating ecosystem-scale responses to climate change.

No abstract

To predict forest response to long-term climate change with high confidence requires that dynamic global vegetation models (DGVMs) be successfully tested against ecosystem response to short-term variations in environmental drivers, including regular seasonal patterns. Here, we used an integrated dataset from four forests in the Brasil flux network, spanning a range of dry-season intensities and lengths, to determine how well four state-of-the-art models (IBIS, ED2, JULES, and CLM3.5) simulated the seasonality of carbon exchanges in Amazonian tropical forests. We found that most DGVMs poorly represented the annual cycle of gross primary productivity (GPP), of photosynthetic capacity (Pc), and of other fluxes and pools. Models simulated consistent dry-season declines in GPP in the equatorial Amazon (Manaus K34, Santarem K67, and Caxiuanã CAX); a contrast to observed GPP increases. Model simulated dry-season GPP reductions were driven by an external environmental factor, 'soil water stress' and consequently by a constant or decreasing photosynthetic infrastructure (Pc), while observed dry-season GPP resulted from a combination of internal biological (leaf-flush and abscission and increased Pc) and environmental (incoming radiation) causes. Moreover, we found models generally overestimated observed seasonal net ecosystem exchange (NEE) and respiration (R ) at equatorial locations. In contrast, a southern Amazon forest (Jarú RJA) exhibited dry-season declines in GPP and R consistent with most DGVMs simulations. While water limitation was represented in models and the primary driver of seasonal photosynthesis in southern Amazonia, changes in internal biophysical processes, light-harvesting adaptations (e.g., variations in leaf area index (LAI) and increasing leaf-level assimilation rate related to leaf demography), and allocation lags between leaf and wood, dominated equatorial Amazon carbon flux dynamics and were deficient or absent from current model formulations. Correctly simulating flux seasonality at tropical forests requires a greater understanding and the incorporation of internal biophysical mechanisms in future model developments.

Satellite and tower-based metrics of forest-scale photosynthesis generally increase with dry season progression across central Amazônia, but the underlying mechanisms lack consensus. We conducted demographic surveys of leaf age composition, and measured the age dependence of leaf physiology in broadleaf canopy trees of abundant species at a central eastern Amazon site. Using a novel leaf-to-branch scaling approach, we used these data to independently test the much-debated hypothesis - arising from satellite and tower-based observations - that leaf phenology could explain the forest-scale pattern of dry season photosynthesis. Stomatal conductance and biochemical parameters of photosynthesis were higher for recently mature leaves than for old leaves. Most branches had multiple leaf age categories simultaneously present, and the number of recently mature leaves increased as the dry season progressed because old leaves were exchanged for new leaves. These findings provide the first direct field evidence that branch-scale photosynthetic capacity increases during the dry season, with a magnitude consistent with increases in ecosystem-scale photosynthetic capacity derived from flux towers. Interactions between leaf age-dependent physiology and shifting leaf age-demographic composition are sufficient to explain the dry season photosynthetic capacity pattern at this site, and should be considered in vegetation models of tropical evergreen forests.