José Luís C. Camargo

Long-term decline of the Amazon carbon sink

Atmospheric carbon dioxide records indicate that the land surface has acted as a strong global carbon sink over recent decades, with a substantial fraction of this sink probably located in the tropics, particularly in the Amazon. Nevertheless, it is unclear how the terrestrial carbon sink will evolve as climate and atmospheric composition continue to change. Here we analyse the historical evolution of the biomass dynamics of the Amazon rainforest over three decades using a distributed network of 321 plots. While this analysis confirms that Amazon forests have acted as a long-term net biomass sink, we find a long-term decreasing trend of carbon accumulation. Rates of net increase in above-ground biomass declined by one-third during the past decade compared to the 1990s. This is a consequence of growth rate increases levelling off recently, while biomass mortality persistently increased throughout, leading to a shortening of carbon residence times. Potential drivers for the mortality increase include greater climate variability, and feedbacks of faster growth on mortality, resulting in shortened tree longevity. The observed decline of the Amazon sink diverges markedly from the recent increase in terrestrial carbon uptake at the global scale, and is contrary to expectations based on models.

Long-term changes in liana abundance and forest dynamics in undisturbed Amazonian forests

Lianas (climbing woody vines) are important structural parasites of tropical trees and may be increasing in abundance in response to global-change drivers. We assessed long-term (-14-year) changes in liana abundance and forest dynamics within 36 1-ha permanent plots spanning -600 km2 of undisturbed rainforest in central Amazonia. Within each plot, we counted each liana stem (> or = 2 cm diameter) and measured its diameter at 1.3 m height, and then used these data to estimate liana aboveground biomass. An initial liana survey was completed in 1997-1999 and then repeated in 2012, using identical methods. Liana abundance in the plots increased by an average of 1.00% +/- 0.88% per year, leading to a highly significant (t = 6.58, df = 35, P < 0.00001) increase in liana stem numbers. Liana biomass rose more slowly over time (0.32% +/- 1.37% per year) and the mean difference between the two sampling intervals was nonsignificant (t = 1.46, df = 35, P = 0.15; paired t tests). Liana size distributions shifted significantly (chi2 = 191, df = 8, P < 0.0001; Chi-square test for independence) between censuses, mainly as a result of a nearly 40% increase in the number of smaller (2-3 cm diameter) lianas, suggesting that lianas recruited rapidly during the study. We used long-term data on rainfall and forest dynamics from our study site to test hypotheses about potential drivers of change in liana communities. Lianas generally increase with rainfall seasonality, but we found no significant trends over time (1997-2012) in five rainfall parameters (total annual rainfall, dry-season rainfall, wet-season rainfall, number of very dry months, CV of monthly rainfall). However, rates of tree mortality and recruitment have increased significantly over time in our plots, and general linear mixed-effect models suggested that lianas were more abundant at sites with higher tree mortality and flatter topography. Rising concentrations of atmospheric CO2, which may stimulate liana growth, might also have promoted liana increases. Our findings clearly support the view that lianas are increasing in abundance in old-growth tropical forests, possibly in response to accelerating forest dynamics and rising CO2 concentrations. The aboveground biomass of trees was lowest in plots with abundant lianas, suggesting that lianas could reduce forest carbon storage and potentially alter forest dynamics if they continue to proliferate.

Variation in stem mortality rates determines patterns of above-ground biomass in Amazonian forests: implications for dynamic global vegetation models

Abstract Understanding the processes that determine above‐ground biomass (AGB) in Amazonian forests is important for predicting the sensitivity of these ecosystems to environmental change and for designing and evaluating dynamic global vegetation models (DGVMs). AGB is determined by inputs from woody productivity [woody net primary productivity (NPP)] and the rate at which carbon is lost through tree mortality. Here, we test whether two direct metrics of tree mortality (the absolute rate of woody biomass loss and the rate of stem mortality) and/or woody NPP, control variation in AGB among 167 plots in intact forest across Amazonia. We then compare these relationships and the observed variation in AGB and woody NPP with the predictions of four DGVMs. The observations show that stem mortality rates, rather than absolute rates of woody biomass loss, are the most important predictor of AGB, which is consistent with the importance of stand size structure for determining spatial variation in AGB. The relationship between stem mortality rates and AGB varies among different regions of Amazonia, indicating that variation in wood density and height/diameter relationships also influences AGB. In contrast to previous findings, we find that woody NPP is not correlated with stem mortality rates and is weakly positively correlated with AGB. Across the four models, basin‐wide average AGB is similar to the mean of the observations. However, the models consistently overestimate woody NPP and poorly represent the spatial patterns of both AGB and woody NPP estimated using plot data. In marked contrast to the observations, DGVMs typically show strong positive relationships between woody NPP and AGB. Resolving these differences will require incorporating forest size structure, mechanistic models of stem mortality and variation in functional composition in DGVMs.

Responses of seedling transplants to environmental variations in contrasting habitats of Central Amazonia

In the Central Amazon we investigated whether seedling performance (survival, and relative growth rates in height and leaf numbers) was affected by initial seedling size (height and leaf numbers) in habitats that varied in their degree of human disturbance: cattle pasture, young secondary forest, 1-ha forest fragment and old-growth forest. Additionally, effects of photosynthetically active radiation (PAR), litter standing crop (LSC) and insect herbivory were evaluated 12 mo after transplantation in seedlings from the native canopy trees Chrysophyllum pomiferum, Micropholis venulosa and Pouteria caimito. Seedling performance changed rank across the understorey environment depending on species. Seedlings of Chrysophyllum thrived in all conditions but under high PAR, Micropholis thrived only in intermediate light conditions, whereas Pouteria thrived under high PAR. Effects of initial seedling size, PAR and herbivory after 1 y were specific to species, whereas LSC had no effect on performance. Initially larger seedlings resulted in lower survival for Chrysophyllum and Pouteria. Herbivory affected seedling performance in all species. Negative effects of herbivory were intensified under low PAR. Overall, our results showed that, as seedlings, species of the same family and characteristic of old-growth forests respond differently to the environmental constraints present in contrasting human-disturbed conditions. Larger seedlings may not always present greater tolerance to physical and biotic mortality risks.

An Amazonian rainforest and its fragments as a laboratory of global change

We synthesize findings from one of the worlds largest and longest‐running experimental investigations, the Biological Dynamics of Forest Fragments Project (BDFFP). Spanning an area of ∼1000 km2 in central Amazonia, the BDFFP was initially designed to evaluate the effects of fragment area on rainforest biodiversity and ecological processes. However, over its 38‐year history to date the project has far transcended its original mission, and now focuses more broadly on landscape dynamics, forest regeneration, regional‐ and global‐change phenomena, and their potential interactions and implications for Amazonian forest conservation. The project has yielded a wealth of insights into the ecological and environmental changes in fragmented forests. For instance, many rainforest species are naturally rare and hence are either missing entirely from many fragments or so sparsely represented as to have little chance of long‐term survival. Additionally, edge effects are a prominent driver of fragment dynamics, strongly affecting forest microclimate, tree mortality, carbon storage and a diversity of fauna.

Apparent environmental synergism drives the dynamics of Amazonian forest fragments

Many contemporary ecosystems are likely to be affected by multiple environmental drivers, complicating efforts to predict future changes in those ecosystems. We studied long-term changes (1980–2012) in forest dynamics and liana (woody vine) abundance and biomass in fragmented and intact forests of the central Amazon. We did so by contrasting trends in 33 permanent 1-ha plots near forest edges (plot center <100 m from the nearest edge) with those in 36 1-ha plots in intact-forest interiors (150–3300 m from nearest edge). In fragmented and edge-affected forests, rates of tree (≥10 cm diameter at breast height) mortality and recruitment were often sharply elevated, especially in the first 10–15 years after fragmentation. Lianas (≥2 cm stem diameter) also increased markedly in abundance (mean ± SD = 1.78 ± 1.23% per yr) and biomass (1.30 ± 1.39% per yr) over time, especially in plots with high edge-related tree mortality. However, plots in undisturbed forest interiors, which were originally established as experimental controls, also experienced long-term changes. In these plots, tree mortality and recruitment rose significantly over time, as did liana abundance (1.00 ± 0.88% per yr) and biomass (0.32 ± 1.37% per yr). These changes were smaller in magnitude than those in fragments but were nonetheless concerted in nature and highly statistically significant. The causes of these changes in forest interiors are unknown, but are broadly consistent with those expected from rising atmospheric CO2 or regional climate drivers that influence forest dynamics. Hence, the dynamics of Amazonian forest fragments cannot be understood simply as a consequence of forest fragmentation. Rather, the changes we observed appear to arise from an interaction of fragmentation with one or more global- or regional-scale drivers affecting forest dynamics. Both sets of phenomena are evidently increasing forest dynamics and liana abundances in fragmented forests, changes that could reduce carbon storage and alter many aspects of forest ecology.

Phylogenetic Impoverishment of Amazonian Tree Communities in an Experimentally Fragmented Forest Landscape

Amazonian rainforests sustain some of the richest tree communities on Earth, but their ecological and evolutionary responses to human threats remain poorly known. We used one of the largest experimental datasets currently available on tree dynamics in fragmented tropical forests and a recent phylogeny of angiosperms to test whether tree communities have lost phylogenetic diversity since their isolation about two decades previously. Our findings revealed an overall trend toward phylogenetic impoverishment across the experimentally fragmented landscape, irrespective of whether tree communities were in 1-ha, 10-ha, or 100-ha forest fragments, near forest edges, or in continuous forest. The magnitude of the phylogenetic diversity loss was low (<2% relative to before-fragmentation values) but widespread throughout the study landscape, occurring in 32 of 40 1-ha plots. Consistent with this loss in phylogenetic diversity, we observed a significant decrease of 50% in phylogenetic dispersion since forest isolation, irrespective of plot location. Analyses based on tree genera that have significantly increased (28 genera) or declined (31 genera) in abundance and basal area in the landscape revealed that increasing genera are more phylogenetically related than decreasing ones. Also, the loss of phylogenetic diversity was greater in tree communities where increasing genera proliferated and decreasing genera reduced their importance values, suggesting that this taxonomic replacement is partially underlying the phylogenetic impoverishment at the landscape scale. This finding has clear implications for the current debate about the role human-modified landscapes play in sustaining biodiversity persistence and key ecosystem services, such as carbon storage. Although the generalization of our findings to other fragmented tropical forests is uncertain, it could negatively affect ecosystem productivity and stability and have broader impacts on coevolved organisms.

Predicted trajectories of tree community change in Amazonian rainforest fragments

&NA; A great challenge for ecologists is predicting how communities in fragmented tropical landscapes will change in the future. Available evidence suggests that fragmented tropical tree communities are progressing along a trajectory of ‘retrogressive succession’, in which the community shifts towards an early or mid‐successional state that will persist indefinitely. Here, we investigate the potential endpoint of retrogressive succession, examining whether it will eventually lead to the highly depauperate communities that characterise recently abandoned agricultural lands. We tested this hypothesis by using neural networks to construct an empirical model of Amazonian rainforest‐tree‐community responses to experimental habitat fragmentation. The strongest predictor of tree‐community composition in the future was its composition in the present, modified by variables like the composition of the surrounding habitat matrix and distance to forest edge. We extrapolated network predictions over a 100 yr period and quantified trajectories of forest communities in multidimensional ordination space. We found no evidence that forest communities, including those near forest edges, were converging strongly towards a composition dominated by just one or two early successional genera. Retrogressive succession may well be stronger in fragmented landscapes altered by chronic disturbances, such as edge‐related fires, selective logging, or intense windstorms, but in this experimental landscape in which other human disturbances are very limited, it is unlikely that forest edge communities will fully revert to the species poor assemblages observed in very early successional landscapes.

Near Infrared Spectroscopy Facilitates Rapid Identification of Both Young and Mature Amazonian Tree Species

Precise identification of plant species requires a high level of knowledge by taxonomists and presence of reproductive material. This represents a major limitation for those working with seedlings and juveniles, which differ morphologically from adults and do not bear reproductive structures. Near-infrared spectroscopy (FT-NIR) has previously been shown to be effective in species discrimination of adult plants, so if young and adults have a similar spectral signature, discriminant functions based on FT-NIR spectra of adults can be used to identify leaves from young plants. We tested this with a sample of 419 plants in 13 Amazonian species from the genera Protium and Crepidospermum (Burseraceae). We obtained 12 spectral readings per plant, from adaxial and abaxial surfaces of dried leaves, and compared the rate of correct predictions of species with discriminant functions for different combinations of readings. We showed that the best models for predicting species in early developmental stages are those containing spectral data from both young and adult plants (98% correct predictions of external samples), but even using only adult spectra it is still possible to attain good levels of identification of young. We obtained an average of 75% correct identifications of young plants by discriminant equations based only on adults, when the most informative wavelengths were selected. Most species were accurately predicted (75–100% correct identifications), and only three had poor predictions (27–60%). These results were obtained despite the fact that spectra of young individuals were distinct from those of adults when species were analyzed individually. We concluded that FT-NIR has a high potential in the identification of species even at different ontogenetic stages, and that young plants can be identified based on spectra of adults with reasonable confidence.

Fragmentation affects plant community composition over time

&NA; Habitat fragmentation can lead to major changes in community composition, but little is known about the dynamics of these changes, or how community trajectories are affected by the initial state of habitat maturity. We use four landscape‐scale experiments from different biogeographic regions to understand how plant community composition responds to fragmentation over decades. Within each experiment, we consider first whether plant communities in the most‐fragmented treatments diverge in composition from plant communities in the least‐fragmented treatments. Second, because communities embedded in different fragments may become more similar to one another over time (biotic homogenization), we asked whether beta diversity – compositional variation across space – declines among fragments over time. Third, we assessed whether fragmentation alters the degree to which temporal change in fragmented landscapes is due to ordered species losses and gains (nestedness) versus species replacements (turnover). For each of these three questions, we contrasted patterns of compositional change in mature communities following fragmentation (disassembly; n = 2 experiments) with patterns in newly‐developing plant communities in fragments cleared of vegetation (assembly; n = 2 experiments). In the two studies where communities were disassembling, community composition in the most‐fragmented habitats diverged from that in least‐fragmented habitats. Beta diversity within a fragmentation treatment did not change over time at any of the four sites. In all four experiments, temporal patterns of compositional change were due mostly to species turnover, although nestedness played a role in the least‐fragmented sites in two of the studies. Overall, the impacts on community composition varied among landscape experiments, and divergence may have been affected by the maturity of the plant community. Future comparisons across ecosystems that account for species identities (vs simply richness) will be critical for predicting the effects of fragmentation, managing mature plant communities in remnants, and restoring plant communities where habitat has been lost.