Asynchronous carbon sink saturation in African and Amazonian tropical forests.

Structurally intact tropical forests sequestered about half of the global terrestrial carbon uptake over the 1990s and early 2000s, removing about 15 per cent of anthropogenic carbon dioxide emissions1-3. Climate-driven vegetation models typically predict that this tropical forest 'carbon sink' will continue for decades4,5. Here we assess trends in the carbon sink using 244 structurally intact African tropical forests spanning 11 countries, compare them with 321 published plots from Amazonia and investigate the underlying drivers of the trends. The carbon sink in live aboveground biomass in intact African tropical forests has been stable for the three decades to 2015, at 0.66 tonnes of carbon per hectare per year (95 per cent confidence interval 0.53-0.79), in contrast to the long-term decline in Amazonian forests6. Therefore the carbon sink responses of Earth's two largest expanses of tropical forest have diverged. The difference is largely driven by carbon losses from tree mortality, with no detectable multi-decadal trend in Africa and a long-term increase in Amazonia. Both continents show increasing tree growth, consistent with the expected net effect of rising atmospheric carbon dioxide and air temperature7-9. Despite the past stability of the African carbon sink, our most intensively monitored plots suggest a post-2010 increase in carbon losses, delayed compared to Amazonia, indicating asynchronous carbon sink saturation on the two continents. A statistical model including carbon dioxide, temperature, drought and forest dynamics accounts for the observed trends and indicates a long-term future decline in the African sink, whereas the Amazonian sink continues to weaken rapidly. Overall, the uptake of carbon into Earth's intact tropical forests peaked in the 1990s. Given that the global terrestrial carbon sink is increasing in size, independent observations indicating greater recent carbon uptake into the Northern Hemisphere landmass10 reinforce our conclusion that the intact tropical forest carbon sink has already peaked. This saturation and ongoing decline of the tropical forest carbon sink has consequences for policies intended to stabilize Earth's climate.

The role of ecosystem transpiration in creating alternate moisture regimes by influencing atmospheric moisture convergence.

The terrestrial water cycle links the soil and atmosphere moisture reservoirs through four fluxes: precipitation, evaporation, runoff, and atmospheric moisture convergence (net import of water vapor to balance runoff). Each of these processes is essential for sustaining human and ecosystem well-being. Predicting how the water cycle responds to changes in vegetation cover remains a challenge. Recently, changes in plant transpiration across the Amazon basin were shown to be associated disproportionately with changes in rainfall, suggesting that even small declines in transpiration (e.g., from deforestation) would lead to much larger declines in rainfall. Here, constraining these findings by the law of mass conservation, we show that in a sufficiently wet atmosphere, forest transpiration can control atmospheric moisture convergence such that increased transpiration enhances atmospheric moisture import and results in water yield. Conversely, in a sufficiently dry atmosphere increased transpiration reduces atmospheric moisture convergence and water yield. This previously unrecognized dichotomy can explain the otherwise mixed observations of how water yield responds to re-greening, as we illustrate with examples from China's Loess Plateau. Our analysis indicates that any additional precipitation recycling due to additional vegetation increases precipitation but decreases local water yield and steady-state runoff. Therefore, in the drier regions/periods and early stages of ecological restoration, the role of vegetation can be confined to precipitation recycling, while once a wetter stage is achieved, additional vegetation enhances atmospheric moisture convergence and water yield. Recent analyses indicate that the latter regime dominates the global response of the terrestrial water cycle to re-greening. Evaluating the transition between regimes, and recognizing the potential of vegetation for enhancing moisture convergence, are crucial for characterizing the consequences of deforestation as well as for motivating and guiding ecological restoration.

Combining camera trap surveys and IUCN range maps to improve knowledge of species distributions.

Reliable maps of species distributions are fundamental for biodiversity research and conservation. The International Union for Conservation of Nature (IUCN) range maps are widely recognized as authoritative representations of species' geographic limits, yet they might not always align with actual occurrence data. In recent area of habitat (AOH) maps, areas that are not habitat have been removed from IUCN ranges to reduce commission errors, but their concordance with actual species occurrence also remains untested. We tested concordance between occurrences recorded in camera trap surveys and predicted occurrences from the IUCN and AOH maps for 510 medium- to large-bodied mammalian species in 80 camera trap sampling areas. Across all areas, cameras detected only 39% of species expected to occur based on IUCN ranges and AOH maps; 85% of the IUCN only mismatches occurred within 200 km of range edges. Only 4% of species occurrences were detected by cameras outside IUCN ranges. The probability of mismatches between cameras and the IUCN range was significantly higher for smaller-bodied mammals and habitat specialists in the Neotropics and Indomalaya and in areas with shorter canopy forests. Our findings suggest that range and AOH maps rarely underrepresent areas where species occur, but they may more often overrepresent ranges by including areas where a species may be absent, particularly at range edges. We suggest that combining range maps with data from ground-based biodiversity sensors, such as camera traps, provides a richer knowledge base for conservation mapping and planning.

Combinación de censos con fototrampas y mapas de extensión de la UICN para incrementar el conocimiento sobre la distribución de las especies Resumen Los mapas confiables de la distribución de las especies son fundamentales para la investigación y conservación de la biodiversidad. Los mapas de distribución de la Unión Internacional para la Conservación de la Naturaleza (UICN) están reconocidos como representaciones de autoridad de los límites geográficos de las especies, aunque no siempre se alinean con los datos actuales de su presencia. En los mapas recientes de área de hábitat (ADH), las áreas que no son hábitat han sido eliminadas de la distribución de la UICN para reducir los errores de comisión, pero su concordancia con la presencia actual de las especies tampoco ha sido analizada. Analizamos la concordancia entre la presencia registrada por los censos de fototrampas y pronosticamos la presencia a partir de los mapas de la UICN y de ADH de 510 especies de mamíferos de talla mediana a grande en 80 áreas de muestreo de fototrampas. Las cámaras detectaron sólo el 39% de las especies esperadas con base en la distribución de la UICN y los mapas de ADH en todas las áreas; el 85% de las disparidades con la UICN ocurrieron dentro de los 200 km a partir del borde de la distribución. Sólo el 4% de la presencia de las especies fue detectada por las cámaras ubicadas fuera de la distribución de la UICN. La probabilidad de disparidad entre las cámaras y la UICN fue significativamente mayor para los mamíferos de talla pequeña y para los especialistas de hábitat en las regiones Neotropical e Indomalaya y en áreas con doseles forestales más bajos. Nuestros hallazgos sugieren que los mapas de distribución y ADH pocas veces subrepresentan las áreas con presencia de las especies, pero con frecuencia pueden sobrerrepresentar la distribución al incluir áreas en donde las especies pueden estar ausentes, en particular los bordes de la distribución. Sugerimos que la combinación de los mapas de distribución con los sensores de biodiversidad en tierra, como las fototrampas, proporciona una base más rica de conocimiento para el mapeo y la planeación de la conservación.

Occupancy winners in tropical protected forests: a pantropical analysis.

The structure of forest mammal communities appears surprisingly consistent across the continental tropics, presumably due to convergent evolution in similar environments. Whether such consistency extends to mammal occupancy, despite variation in species characteristics and context, remains unclear. Here we ask whether we can predict occupancy patterns and, if so, whether these relationships are consistent across biogeographic regions. Specifically, we assessed how mammal feeding guild, body mass and ecological specialization relate to occupancy in protected forests across the tropics. We used standardized camera-trap data (1002 camera-trap locations and 2-10 years of data) and a hierarchical Bayesian occupancy model. We found that occupancy varied by regions, and certain species characteristics explained much of this variation. Herbivores consistently had the highest occupancy. However, only in the Neotropics did we detect a significant effect of body mass on occupancy: large mammals had lowest occupancy. Importantly, habitat specialists generally had higher occupancy than generalists, though this was reversed in the Indo-Malayan sites. We conclude that habitat specialization is key for understanding variation in mammal occupancy across regions, and that habitat specialists often benefit more from protected areas, than do generalists. The contrasting examples seen in the Indo-Malayan region probably reflect distinct anthropogenic pressures.

Human density modulates spatial associations among tropical forest terrestrial mammal species.

The spatial aggregation of species pairs often increases with the ecological similarity of the species involved. However, the way in which environmental conditions and anthropogenic activity affect the relationship between spatial aggregation and ecological similarity remains unknown despite the potential for spatial associations to affect species interactions, ecosystem function, and extinction risk. Given that human disturbance has been shown to both increase and decrease spatial associations among species pairs, ecological similarity may have a role in mediating these patterns. Here, we test the influences of habitat diversity, primary productivity, human population density, and species' ecological similarity based on functional traits (i.e., functional trait similarity) on spatial associations among tropical forest mammals. Large mammals are highly sensitive to anthropogenic change and therefore susceptible to changes in interspecific spatial associations. Using two-species occupancy models and camera trap data, we quantified the spatial overlap of 1216 species pairs from 13 tropical forest protected areas around the world. We found that the association between ecological similarity and interspecific species associations depended on surrounding human density. Specifically, aggregation of ecologically similar species was more than an order of magnitude stronger in landscapes with the highest human density compared to those with the lowest human density, even though all populations occurred within protected areas. Human-induced changes in interspecific spatial associations have been shown to alter top-down control by predators, increase disease transmission and increase local extinction rates. Our results indicate that anthropogenic effects on the distribution of wildlife within protected areas are already occurring and that impacts on species interactions, ecosystem functions, and extinction risk warrant further investigation.

Rare and common species contribute disproportionately to the functional variation within tropical forests.

Understanding how functional traits and functional entities (FEs, i.e., unique combinations of functional traits) are distributed within plant communities can contribute to the understanding of vegetation properties and changes in species composition. We utilized investigation data on woody plants (including trees, shrubs and lianas) from 17 1-ha plots across six old-growth tropical forest types on Hainan island, China. Plant species were categorized as common (>1 individuals/ha) and rare species (≤1 individuals/ha) according to their abundance to determine how they contributed to different ecosystem functions. First, we assessed the differences in traits between common and rare species, and second, we examined functional redundancy, functional over-redundancy, and functional vulnerability for common and rare species of the forests. We found that both common species and rare species in each of the forest types were placed into just a few FEs, leading to functional over-redundancy and resulting in functional vulnerability. Rare species tended to have different trait values than those of common species, and were differently distributed among FEs, indicating different contributions to ecosystem functioning. Our results highlighted the disproportionate contribution of rare species in all of the studied forests. Rare species are more likely than common species to possess unique FEs, and thus, they have a disproportionately large contribution to community trait space. The loss of such species may impact the functioning, redundancy, and resilience of tropical forests.

Standardized Assessment of Biodiversity Trends in Tropical Forest Protected Areas: The End Is Not in Sight.

Extinction rates in the Anthropocene are three orders of magnitude higher than background and disproportionately occur in the tropics, home of half the world's species. Despite global efforts to combat tropical species extinctions, lack of high-quality, objective information on tropical biodiversity has hampered quantitative evaluation of conservation strategies. In particular, the scarcity of population-level monitoring in tropical forests has stymied assessment of biodiversity outcomes, such as the status and trends of animal populations in protected areas. Here, we evaluate occupancy trends for 511 populations of terrestrial mammals and birds, representing 244 species from 15 tropical forest protected areas on three continents. For the first time to our knowledge, we use annual surveys from tropical forests worldwide that employ a standardized camera trapping protocol, and we compute data analytics that correct for imperfect detection. We found that occupancy declined in 22%, increased in 17%, and exhibited no change in 22% of populations during the last 3-8 years, while 39% of populations were detected too infrequently to assess occupancy changes. Despite extensive variability in occupancy trends, these 15 tropical protected areas have not exhibited systematic declines in biodiversity (i.e., occupancy, richness, or evenness) at the community level. Our results differ from reports of widespread biodiversity declines based on aggregated secondary data and expert opinion and suggest less extreme deterioration in tropical forest protected areas. We simultaneously fill an important conservation data gap and demonstrate the value of large-scale monitoring infrastructure and powerful analytics, which can be scaled to incorporate additional sites, ecosystems, and monitoring methods. In an era of catastrophic biodiversity loss, robust indicators produced from standardized monitoring infrastructure are critical to accurately assess population outcomes and identify conservation strategies that can avert biodiversity collapse.

Convergence of bark investment according to fire and climate structures ecosystem vulnerability to future change.

Fire regimes in savannas and forests are changing over much of the world. Anticipating the impact of these changes requires understanding how plants are adapted to fire. In this study, we test whether fire imposes a broad selective force on a key fire-tolerance trait, bark thickness, across 572 tree species distributed worldwide. We show that investment in thick bark is a pervasive adaptation in frequently burned areas across savannas and forests in both temperate and tropical regions where surface fires occur. Geographic variability in bark thickness is largely explained by annual burned area and precipitation seasonality. Combining environmental and species distribution data allowed us to assess vulnerability to future climate and fire conditions: tropical rainforests are especially vulnerable, whereas seasonal forests and savannas are more robust. The strong link between fire and bark thickness provides an avenue for assessing the vulnerability of tree communities to fire and demands inclusion in global models.

Termites and large herbivores influence seed removal rates in an African savanna.

Seed removal can influence plant community dynamics, composition, and resulting vegetation characteristics. In the African savanna, termites and large herbivores influence vegetation in various ways, likely including indirect effects on seed predators and secondary dispersers. However, the intensity and variation of seed removal rates in African savannas has seldom been studied. We experimentally investigated whether termites and large herbivores were important factors in the mechanisms contributing to observed patterns in tree species composition on and off mounds, in Lake Mburo National Park, Uganda. Within fenced (excluding large herbivores) and unfenced termite mound and adjacent savanna plots, we placed seeds of nine native tree species within small open "cages," accessed by all animals, roofed cages that only allowed access to small vertebrates and invertebrates, and closed cages that permitted access by smaller invertebrates only (5 mm wire mesh). We found that mean seed removal rate was high (up to 87.3% per 3 d). Mound habitats experienced significantly higher removal rates than off-mound habitats. The mean removal rate of native seeds from closed cages was 11.1% per 3 d compared with 19.4% and 23.3% removed per 3 d in the roofed and open cages, respectively. Smaller seeds experienced higher removal rates than larger seeds. Large herbivore exclusion on mounds reduced native seed removal rates by a mean of 8.8% in the open cages, but increased removal rates by 1.7% in the open cages when off-mound habitats were fenced. While removal rates from open cages were higher on active mounds (30.9%) than on inactive mounds (26.7%), the removal rates from closed cages were lower on active vs. inactive mounds (6.1% vs. 11.6%, respectively). Thus, we conclude that large herbivores and Macrotermes mounds influence seed removal rates, though these effects appear indirect.

Limited carbon and biodiversity co-benefits for tropical forest mammals and birds.

The conservation of tropical forest carbon stocks offers the opportunity to curb climate change by reducing greenhouse gas emissions from deforestation and simultaneously conserve biodiversity. However, there has been considerable debate about the extent to which carbon stock conservation will provide benefits to biodiversity in part because whether forests that contain high carbon density in their aboveground biomass also contain high animal diversity is unknown. Here, we empirically examined medium to large bodied ground-dwelling mammal and bird (hereafter "wildlife") diversity and carbon stock levels within the tropics using camera trap and vegetation data from a pantropical network of sites. Specifically, we tested whether tropical forests that stored more carbon contained higher wildlife species richness, taxonomic diversity, and trait diversity. We found that carbon stocks were not a significant predictor for any of these three measures of diversity, which suggests that benefits for wildlife diversity will not be maximized unless wildlife diversity is explicitly taken into account; prioritizing carbon stocks alone will not necessarily meet biodiversity conservation goals. We recommend conservation planning that considers both objectives because there is the potential for more wildlife diversity and carbon stock conservation to be achieved for the same total budget if both objectives are pursued in tandem rather than independently. Tropical forests with low elevation variability and low tree density supported significantly higher wildlife diversity. These tropical forest characteristics may provide more affordable proxies of wildlife diversity for future multi-objective conservation planning when fine scale data on wildlife are lacking.

Ten principles for a landscape approach to reconciling agriculture, conservation, and other competing land uses.

"Landscape approaches" seek to provide tools and concepts for allocating and managing land to achieve social, economic, and environmental objectives in areas where agriculture, mining, and other productive land uses compete with environmental and biodiversity goals. Here we synthesize the current consensus on landscape approaches. This is based on published literature and a consensus-building process to define good practice and is validated by a survey of practitioners. We find the landscape approach has been refined in response to increasing societal concerns about environment and development tradeoffs. Notably, there has been a shift from conservation-orientated perspectives toward increasing integration of poverty alleviation goals. We provide 10 summary principles to support implementation of a landscape approach as it is currently interpreted. These principles emphasize adaptive management, stakeholder involvement, and multiple objectives. Various constraints are recognized, with institutional and governance concerns identified as the most severe obstacles to implementation. We discuss how these principles differ from more traditional sectoral and project-based approaches. Although no panacea, we see few alternatives that are likely to address landscape challenges more effectively than an approach circumscribed by the principles outlined here.

Increasing carbon storage in intact African tropical forests.

The response of terrestrial vegetation to a globally changing environment is central to predictions of future levels of atmospheric carbon dioxide. The role of tropical forests is critical because they are carbon-dense and highly productive. Inventory plots across Amazonia show that old-growth forests have increased in carbon storage over recent decades, but the response of one-third of the world's tropical forests in Africa is largely unknown owing to an absence of spatially extensive observation networks. Here we report data from a ten-country network of long-term monitoring plots in African tropical forests. We find that across 79 plots (163 ha) above-ground carbon storage in live trees increased by 0.63 Mg C ha(-1) yr(-1) between 1968 and 2007 (95% confidence interval (CI), 0.22-0.94; mean interval, 1987-96). Extrapolation to unmeasured forest components (live roots, small trees, necromass) and scaling to the continent implies a total increase in carbon storage in African tropical forest trees of 0.34 Pg C yr(-1) (CI, 0.15-0.43). These reported changes in carbon storage are similar to those reported for Amazonian forests per unit area, providing evidence that increasing carbon storage in old-growth forests is a pan-tropical phenomenon. Indeed, combining all standardized inventory data from this study and from tropical America and Asia together yields a comparable figure of 0.49 Mg C ha(-1) yr(-1) (n = 156; 562 ha; CI, 0.29-0.66; mean interval, 1987-97). This indicates a carbon sink of 1.3 Pg C yr(-1) (CI, 0.8-1.6) across all tropical forests during recent decades. Taxon-specific analyses of African inventory and other data suggest that widespread changes in resource availability, such as increasing atmospheric carbon dioxide concentrations, may be the cause of the increase in carbon stocks, as some theory and models predict.

Soils on exposed Sunda shelf shaped biogeographic patterns in the equatorial forests of Southeast Asia.

The marked biogeographic difference between western (Malay Peninsula and Sumatra) and eastern (Borneo) Sundaland is surprising given the long time that these areas have formed a single landmass. A dispersal barrier in the form of a dry savanna corridor during glacial maxima has been proposed to explain this disparity. However, the short duration of these dry savanna conditions make it an unlikely sole cause for the biogeographic pattern. An additional explanation might be related to the coarse sandy soils of central Sundaland. To test these two nonexclusive hypotheses, we performed a floristic cluster analysis based on 111 tree inventories from Peninsular Malaysia, Sumatra, and Borneo. We then identified the indicator genera for clusters that crossed the central Sundaland biogeographic boundary and those that did not cross and tested whether drought and coarse-soil tolerance of the indicator genera differed between them. We found 11 terminal floristic clusters, 10 occurring in Borneo, 5 in Sumatra, and 3 in Peninsular Malaysia. Indicator taxa of clusters that occurred across Sundaland had significantly higher coarse-soil tolerance than did those from clusters that occurred east or west of central Sundaland. For drought tolerance, no such pattern was detected. These results strongly suggest that exposed sandy sea-bed soils acted as a dispersal barrier in central Sundaland. However, we could not confirm the presence of a savanna corridor. This finding makes it clear that proposed biogeographic explanations for plant and animal distributions within Sundaland, including possible migration routes for early humans, need to be reevaluated.

Pseudoreplication in tropical forests and the resulting effects on biodiversity conservation.

Tropical forest ecosystems are threatened by habitat conversion and other anthropogenic actions. Timber production forests can augment the conservation value of primary forest reserves, but studies of logging effects often yield contradictory findings and thus inhibit efforts to develop clear conservation strategies. We hypothesized that much of this variability reflects a common methodological flaw, simple pseudoreplication, that confounds logging effects with preexisting spatial variation. We reviewed recent studies of the effects of logging on biodiversity in tropical forests (n = 77) and found that 68% were definitively pseudoreplicated while only 7% were definitively free of pseudoreplication. The remaining proportion could not be clearly categorized. In addition, we collected compositional data on 7 taxa in 24 primary forest research plots and systematically analyzed subsets of these plots to calculate the probability that a pseudoreplicated comparison would incorrectly identify a treatment effect. Rates of false inference (i.e., the spurious detection of a treatment effect) were >0.5 for 2 taxa, 0.3-0.5 for 2 taxa, and <0.3 for 3 taxa. Our findings demonstrate that tropical conservation strategies are being informed by a body of literature that is rife with unwarranted inferences. Addressing pseudoreplication is essential for accurately assessing biodiversity in logged forests, identifying the relative merits of specific management practices and landscape configurations, and effectively balancing conservation with timber production in tropical forests.

Accessing local knowledge to identify where species of conservation concern occur in a tropical forest landscape.

Conventional biodiversity surveys play an important role in ensuring good conservation friendly management in tropical forest regions but are demanding in terms of expertise, time, and budget. Can local people help? Here, we illustrate how local knowledge can support low cost conservation surveys. We worked in the Malinau watershed, East Kalimantan, Indonesia, an area currently at risk of extensive forest loss. We selected eight species of regional conservation interest: rafflesia (Rafflesia spp.), black orchid (Coelogyne pandurata), sun bear (Helarctos malayanus), tarsier (Tarsius bancanus), slow loris (Nycticebus coucang), proboscis monkey (Nasalis larvatus), clouded leopard (Neofelis diardi/N. nebulosa), and orang-utan (Pongo pygmaeus). We asked 52 informants in seven villages if, where and when they had observed these species. We used maps, based on both geo-referenced and sketched features, to record these observations. Verification concerns and related issues are discussed. Evaluations suggest our local information is reliable. Our study took 6 weeks and cost about USD 5000. Extensive expert based field surveys across the same region would cost one or two orders of magnitude more. The records extend the known distribution for sun bear, tarsier, slow loris, and clouded leopard. Reports of rafflesia, proboscis monkey, and orang-utan are of immediate conservation significance. While quality concerns should never be abandoned, we conclude that local people can help expand our knowledge of large areas in an effective, reliable, and low cost manner and thus contribute to improved management.