Long-term Ecological Research: Chasing fashions or being prepared for fashion changes?

Long-term-ecological-research (LTER) faces many challenges, including the difficulty of obtaining long-term funding, changes in research questions and sampling designs, keeping researchers collecting standardized data for many years, impediments to interactions with local people, and the difficulty of integrating the needs of local decision makers with "big science". These issues result in a lack of universally accepted guidelines as to how research should be done and integrated among LTER sites. Here we discuss how the RAPELD (standardized field infrastructure system), can help deal with these issues as a complementary technique in LTER studies, allowing comparisons across landscapes and ecosystems and reducing sampling costs. RAPELD uses local surveys to understand broad spatial and temporal patterns while enhancing decision-making and training of researchers, local indigenous groups and traditional communities. Sampling of ecological data can be carried out by different researchers through standardized protocols, resulting in spatial data that can be used to answer temporal questions, and allow new questions to be investigated. Results can also be integrated into existing biodiversity networks. Integrated systems are the most efficient way to save resources, maximize results, and accumulate information that can be used in the face of the unknown unknowns upon which our future depends.

Long-term standardized ecological research in an Amazonian savanna: a laboratory under threat.

A few decades ago, researchers from the National Institute for Amazonian Research (INPA) started a pilot study to integrate the ecological studies of several organisms using monitoring plots, which then became the embryo for the creation of the RAPELD (Rapid Assessments and Long-term Ecological Research) system used by the Program for Biodiversity Research (PPBio) and the Long-term ecological research site POPA (PELD Western Pará). They installed and maintained permanent plots in an Amazonian-savanna patch near to the village of Alter do Chão. Amazonian savannas constitute a threatened ecosystem comprising only 6% of the Amazon biome. Most of the studies focused on three main long-term ecological research questions, but the site was also of importance for other inquiries and for the training of young researchers, contributing 71 articles so far and 32 masters and doctorate theses. Here, we present the experimental design and results of standardized studies in the savannas and forest fragments near Alter do Chão that have been carried out over the years. We discuss the future prospects and local threats to the area (e.g. soy crops and land speculation), and highlight the need to incorporate Alter do Chão villagers in land-use planning in the region.

Feeding of Arapaima sp.: integrating stomach contents and local ecological knowledge.

The giant arapaima (Arapaima sp.) has been described as a fish of change in Amazonia because of its important role in the conservation of floodplains, food security and income generation for rural communities. Nonetheless, despite the cultural, ecological and economic importance of arapaima, data on diet are scarce. Aiming to expand knowledge about arapaima diet in western Amazonia, scientific knowledge was integrated with the knowledge of local dwellers. During the low-water period (September 2018) and the falling-water period (June 2019), arapaima stomachs were collected from 11 floodplain lakes in the middle Juruá River. All fishes were measured [TL (total length)] and sexed. Food items from each stomach were categorized as fishes, invertebrates, plants and bone remains and weighed. Also, in the latter period, experienced local fishers were interviewed about arapaima feeding. This integrated approach revealed that young arapaima eat fish and invertebrates but adult arapaima eat fish of a wide range of species, which were mainly of low and intermediate trophic positions. This study reports the first case of cannibalism for arapaima and also shows that during the low-water period, many individuals had empty stomachs or only some small fish-bone remains and/or plant material. Arapaima sex and TL had no influence on the absence of prey in stomach contents. Overall, it can be concluded that local people had consistent ethnobiological knowledge of arapaima feeding ecology that could be useful within management projects in the region.

Biodiversity: the chasm between what we know and we need to know.

In this review I focus on what we need to know to make decisions relevant to land-use planning. I discuss four questions: What information about the distribution of biodiversity is available to decision makers? What sort of information is required at a local scale? Can we use species-distribution modeling to compensate for the lack of empirical information at larger scales? Can we use surrogates based on remote sensing for all our decisions? To be effective, biodiversity information needs to be based on standardized sampling with data made available during the initial planning phases of infrastructure projects, which are now based only on engineering or social considerations and occur several decades before construction starts. The RAPELD method is now being used in many environmental-impact studies to generate standardized data, but there is presently no mechanism to include biodiversity information in the initial phases of decision making, and this has unfavorable consequences for economic development and the environment.

From a bat's perspective, protected riparian areas should be wider than defined by Brazilian laws.

Riparian areas around streams are those areas in which biological communites are directly influenced by the stream. The size of protected riparian areas and their conservation has become a controversial topic after changes implemented in the Brazilian Forest Code (BFC): a set of laws that regulates the size of Permanent Protection Areas (PPA). Here, we investigate the influence of distance from water bodies on bat-species and guild composition in a lowland Amazonian rainforest. Our hypotheses were that bat assemblages would change depending on the distance to the water body and that the abundance of herbivorous bats (frugivorous and nectarivorous) would be greater in areas close to water. Bats were captured with mist-nets in 24 riparian and 25 non-riparian plots within a trail grid in an old-growth terra-firme forest, northeast of Manaus, Amazonas, Brazil. Each plot was sampled three times in a total of 7056 net-hours. We captured 1191 bats, comprising 51 species. We used model selection based on AIC (Akaike Information Criterion) to compare linear and piecewise regressions to estimate the ecological thresholds for different bat assemblages. Piecewise models with one breakpoint were more parsimonious than linear models for abundance data, and the species and guild composition of animalivorous and frugivorous bats. Animalivorous-bat abundance increased from the stream to about 181 m, and frugivorous-bat abundance decreased within 50 m of the stream. The patterns of guild abundance suggest that frugivorous bats may need greater access to streams than animalivorous bats. The most conservative model suggests that most of the variation in bat composition occurs close to the stream and extends to up 114 m from the banks. Therefore, the 30 m wide strip of riparian forest protected by Brazilian law would maintain a relatively small fraction of bat-species assemblages in Ducke Reserve, and is insufficient to represent most of the assemblage-composition variation within the riparian zone. The suggestion to reduce the width of the protected riparian zone from 30 to 15 m for streams smaller than 10 m wide, as is under discussion, would likely be prejudicial for bat assemblages.

Extinction risks forced by climatic change and intraspecific variation in the thermal physiology of a tropical lizard.

Temperature increases can impact biodiversity and predicting their effects is one of the main challenges facing global climate-change research. Ectotherms are sensitive to temperature change and, although predictions indicate that tropical species are highly vulnerable to global warming, they remain one of the least studied groups with respect to the extent of physiological variation and local extinction risks. We model the extinction risks for a tropical heliothermic teiid lizard (Kentropyx calcarata) integrating previously obtained information on intraspecific phylogeographic structure, eco-physiological traits and contemporary species distributions in the Amazon rainforest and its ecotone to the Cerrado savannah. We also investigated how thermal-biology traits vary throughout the species' geographic range and the consequences of such variation for lineage vulnerability. We show substantial variation in thermal tolerance of individuals among thermally distinct sites. Thermal critical limits were highly correlated with operative environmental temperatures. Our physiological/climatic model predicted relative extinction risks for local populations within clades of K. calcarata for 2050 ranging between 26.1% and 70.8%, while for 2070, extinction risks ranged from 52.8% to 92.8%. Our results support the hypothesis that tropical-lizard taxa are at high risk of local extinction caused by increasing temperatures. However, the thermo-physiological differences found across the species' distribution suggest that local adaptation may allow persistence of this tropical ectotherm in global warming scenarios. These results will serve as basis to further research to investigate the strength of local adaptation to climate change. Persistence of Kentropyx calcarata also depends on forest preservation, but the Amazon rainforest is currently under high deforestation rates. We argue that higher conservation priority is necessary so the Amazon rainforest can fulfill its capacity to absorb the impacts of temperature increase on tropical ectotherms during climate change.

Estimating species richness in hyper-diverse large tree communities.

Species richness estimation is one of the most widely used analyses carried out by ecologists, and nonparametric estimators are probably the most used techniques to carry out such estimations. We tested the assumptions and results of nonparametric estimators and those of a logseries approach to species richness estimation for simulated tropical forests and five data sets from the field. We conclude that nonparametric estimators are not suitable to estimate species richness in tropical forests, where sampling intensity is usually low and richness is high, because the assumptions of the methods do not meet the sampling strategy used in most studies. The logseries, while also requiring substantial sampling, is much more effective in estimating species richness than commonly used nonparametric estimators, and its assumptions better match the way field data is being collected.

Contrasting Patterns of Gene Flow for Amazonian Snakes That Actively Forage and Those That Wait in Ambush.

Knowledge of genetic structure, geographic distance and environmental heterogeneity can be used to identify environmental features and natural history traits that influence dispersal and gene flow. Foraging mode is a trait that might predict dispersal capacity in snakes, because actively foragers typically have greater movement rates than ambush predators. Here, we test the hypothesis that 2 actively foraging snakes have higher levels of gene flow than 2 ambush predators. We evaluated these 4 co-distributed species of snakes in the Brazilian Amazon. Snakes were sampled along an 880 km transect from the central to the southwest of the Amazon basin, which covered a mosaic of vegetation types and seasonal differences in climate. We analyzed thousands of single nucleotide polymorphisms to compare patterns of neutral gene flow based on isolation by geographic distance (IBD) and environmental resistance (IBR). We show that IBD and IBR were only evident in ambush predators, implying lower levels of dispersal than the active foragers. Therefore, gene flow was high enough in the active foragers analyzed here to prevent any build-up of spatial genotypic structure with respect to geographic distance and environmental heterogeneity.

Toward an integrated monitoring framework to assess the effects of tropical forest degradation and recovery on carbon stocks and biodiversity.

Tropical forests harbor a significant portion of global biodiversity and are a critical component of the climate system. Reducing deforestation and forest degradation contributes to global climate-change mitigation efforts, yet emissions and removals from forest dynamics are still poorly quantified. We reviewed the main challenges to estimate changes in carbon stocks and biodiversity due to degradation and recovery of tropical forests, focusing on three main areas: (1) the combination of field surveys and remote sensing; (2) evaluation of biodiversity and carbon values under a unified strategy; and (3) research efforts needed to understand and quantify forest degradation and recovery. The improvement of models and estimates of changes of forest carbon can foster process-oriented monitoring of forest dynamics, including different variables and using spatially explicit algorithms that account for regional and local differences, such as variation in climate, soil, nutrient content, topography, biodiversity, disturbance history, recovery pathways, and socioeconomic factors. Generating the data for these models requires affordable large-scale remote-sensing tools associated with a robust network of field plots that can generate spatially explicit information on a range of variables through time. By combining ecosystem models, multiscale remote sensing, and networks of field plots, we will be able to evaluate forest degradation and recovery and their interactions with biodiversity and carbon cycling. Improving monitoring strategies will allow a better understanding of the role of forest dynamics in climate-change mitigation, adaptation, and carbon cycle feedbacks, thereby reducing uncertainties in models of the key processes in the carbon cycle, including their impacts on biodiversity, which are fundamental to support forest governance policies, such as Reducing Emissions from Deforestation and Forest Degradation.

Markedly divergent estimates of Amazon forest carbon density from ground plots and satellites.

AIM: The accurate mapping of forest carbon stocks is essential for understanding the global carbon cycle, for assessing emissions from deforestation, and for rational land-use planning. Remote sensing (RS) is currently the key tool for this purpose, but RS does not estimate vegetation biomass directly, and thus may miss significant spatial variations in forest structure. We test the stated accuracy of pantropical carbon maps using a large independent field dataset. LOCATION: Tropical forests of the Amazon basin. The permanent archive of the field plot data can be accessed at: http://dx.doi.org/10.5521/FORESTPLOTS.NET/2014_1. METHODS: Two recent pantropical RS maps of vegetation carbon are compared to a unique ground-plot dataset, involving tree measurements in 413 large inventory plots located in nine countries. The RS maps were compared directly to field plots, and kriging of the field data was used to allow area-based comparisons. RESULTS: The two RS carbon maps fail to capture the main gradient in Amazon forest carbon detected using 413 ground plots, from the densely wooded tall forests of the north-east, to the light-wooded, shorter forests of the south-west. The differences between plots and RS maps far exceed the uncertainties given in these studies, with whole regions over- or under-estimated by > 25%, whereas regional uncertainties for the maps were reported to be < 5%. MAIN CONCLUSIONS: Pantropical biomass maps are widely used by governments and by projects aiming to reduce deforestation using carbon offsets, but may have significant regional biases. Carbon-mapping techniques must be revised to account for the known ecological variation in tree wood density and allometry to create maps suitable for carbon accounting. The use of single relationships between tree canopy height and above-ground biomass inevitably yields large, spatially correlated errors. This presents a significant challenge to both the forest conservation and remote sensing communities, because neither wood density nor species assemblages can be reliably mapped from space.

Vocal repertoire of the social giant otter.

According to the "social intelligence hypothesis," species with complex social interactions have more sophisticated communication systems. Giant otters (Pteronura brasiliensis) live in groups with complex social interactions. It is likely that the vocal communication of giant otters is more sophisticated than previous studies suggest. The objectives of the current study were to describe the airborne vocal repertoire of giant otters in the Pantanal area of Brazil, to analyze call types within different behavioral contexts, and to correlate vocal complexity with level of sociability of mustelids to verify whether or not the result supports the social intelligence hypothesis. The behavior of nine giant otters groups was observed. Vocalizations recorded were acoustically and statistically analyzed to describe the species' repertoire. The repertoire was comprised by 15 sound types emitted in different behavioral contexts. The main behavioral contexts of each sound type were significantly associated with the acoustic variable ordination of different sound types. A strong correlation between vocal complexity and sociability was found for different species, suggesting that the communication systems observed in the family mustelidae support the social intelligence hypothesis.

Blood Biochemical Reference Intervals of Black Caimans (Melanosuchus niger) and Spectacled Caimans (Caiman crocodilus) in the Brazilian Amazon Region.

Reference intervals for physiologic parameters, crucial for assessing the health status of animals, have been documented for various crocodilian species across the globe. Nonetheless, the establishment of plasma biochemical reference intervals specific to Amazonian crocodilians remains incomplete. In an effort to address this gap, we procured blood samples from 65 black caimans (Melanosuchus niger) and 58 spectacled caimans (Caiman crocodilus) during the period of September-December 2019 within the Anavilhanas National Park in the Brazilian Amazon region We aimed to define reference intervals for 11 key plasma variables measured, namely glucose, triglycerides, total cholesterol, calcium, magnesium, sodium, potassium, albumin, total protein, uric acid, and urea. In general, the determined blood reference intervals aligned closely with those established for other crocodilian species. Some specific measurements, such as total cholesterol, sodium, and magnesium, exhibited distinct variations based on the species. Furthermore, female black caimans showcased elevated cholesterol levels compared with their male counterparts. Within the spectacled caimans, disparities related to sex were evident solely in the case of electrolytes sodium and potassium, with males demonstrating higher levels compared with females. These reference intervals not only provide data for assessing potential fluctuations in the health of wild or captive Amazonian crocodilians but also hold value for veterinary management.

Body size predicts ontogenetic nitrogen stable-isotope (δ15N) variation, but has little relationship with trophic level in ectotherm vertebrate predators.

Large predators have disproportionate effects on their underlying food webs. Thus, appropriately assigning trophic positions has important conservation implications both for the predators themselves and for their prey. Large-bodied predators are often referred to as apex predators, implying that they are many trophic levels above primary producers. However, theoretical considerations predict both higher and lower trophic position with increasing body size. Nitrogen stable isotope values (δ15N) are increasingly replacing stomach contents or behavioral observations to assess trophic position and it is often assumed that ontogenetic dietary shifts result in higher trophic positions. Intraspecific studies based on δ15N values found a positive relationship between size and inferred trophic position. Here, we use datasets of predatory vertebrate ectotherms (crocodilians, turtles, lizards and fishes) to show that, although there are positive intraspecific relationships between size and δ15N values, relationships between stomach-content-based trophic level (TPdiet) and size are undetectable or negative. As there is usually no single value for 15N trophic discrimination factor (TDF) applicable to a predator species or its prey, estimates of trophic position based on δ15N in ectotherm vertebrates with large size ranges, may be inaccurate and biased. We urge a reconsideration of the sole use of δ15N values to assess trophic position and encourage the combined use of isotopes and stomach contents to assess diet and trophic level.

One sixth of Amazonian tree diversity is dependent on river floodplains.

Amazonia's floodplain system is the largest and most biodiverse on Earth. Although forests are crucial to the ecological integrity of floodplains, our understanding of their species composition and how this may differ from surrounding forest types is still far too limited, particularly as changing inundation regimes begin to reshape floodplain tree communities and the critical ecosystem functions they underpin. Here we address this gap by taking a spatially explicit look at Amazonia-wide patterns of tree-species turnover and ecological specialization of the region's floodplain forests. We show that the majority of Amazonian tree species can inhabit floodplains, and about a sixth of Amazonian tree diversity is ecologically specialized on floodplains. The degree of specialization in floodplain communities is driven by regional flood patterns, with the most compositionally differentiated floodplain forests located centrally within the fluvial network and contingent on the most extraordinary flood magnitudes regionally. Our results provide a spatially explicit view of ecological specialization of floodplain forest communities and expose the need for whole-basin hydrological integrity to protect the Amazon's tree diversity and its function.

Thermal relations of dwarf caiman, Paleosuchus palpebrosus, in a hillside stream: evidence for an unusual thermal niche among crocodilians.

Body temperatures of 13 Paleosuchus palpebrosus, 7 males and 6 females, were monitored by radio-telemetry during cold periods (dry season) and warm periods (wet and dry seasons) in a stream draining into the Brazilian Pantanal. The mass of the caimans varied from 2.5 to 20.0kg, and snout-vent length from 47.5 to 95.0cm. Mean monthly body temperature was 21.6°C, and varied from 20.1 to 25.6°C throughout the year. Body temperature was correlated with air and water temperature but did not differ between males and females. Unlike all other crocodilians investigated in detail to date, the caimans did not show evidence of attempts to obtain higher body temperatures when ambient temperatures were low, and had low and generally constant temperatures in relation to the surrounding air and water throughout the year. The caimans remained in burrows during cold periods in the dry season, which may explain why they did not seek higher temperatures. Tolerance of relatively low and constant body temperatures may be a key adaptation of species of Paleosuchus, allowing them to occupy environments inhospitable to other crocodilians.

Mapping density, diversity and species-richness of the Amazon tree flora.

Using 2.046 botanically-inventoried tree plots across the largest tropical forest on Earth, we mapped tree species-diversity and tree species-richness at 0.1-degree resolution, and investigated drivers for diversity and richness. Using only location, stratified by forest type, as predictor, our spatial model, to the best of our knowledge, provides the most accurate map of tree diversity in Amazonia to date, explaining approximately 70% of the tree diversity and species-richness. Large soil-forest combinations determine a significant percentage of the variation in tree species-richness and tree alpha-diversity in Amazonian forest-plots. We suggest that the size and fragmentation of these systems drive their large-scale diversity patterns and hence local diversity. A model not using location but cumulative water deficit, tree density, and temperature seasonality explains 47% of the tree species-richness in the terra-firme forest in Amazonia. Over large areas across Amazonia, residuals of this relationship are small and poorly spatially structured, suggesting that much of the residual variation may be local. The Guyana Shield area has consistently negative residuals, showing that this area has lower tree species-richness than expected by our models. We provide extensive plot meta-data, including tree density, tree alpha-diversity and tree species-richness results and gridded maps at 0.1-degree resolution.

More than 10,000 pre-Columbian earthworks are still hidden throughout Amazonia.

Indigenous societies are known to have occupied the Amazon basin for more than 12,000 years, but the scale of their influence on Amazonian forests remains uncertain. We report the discovery, using LIDAR (light detection and ranging) information from across the basin, of 24 previously undetected pre-Columbian earthworks beneath the forest canopy. Modeled distribution and abundance of large-scale archaeological sites across Amazonia suggest that between 10,272 and 23,648 sites remain to be discovered and that most will be found in the southwest. We also identified 53 domesticated tree species significantly associated with earthwork occurrence probability, likely suggesting past management practices. Closed-canopy forests across Amazonia are likely to contain thousands of undiscovered archaeological sites around which pre-Columbian societies actively modified forests, a discovery that opens opportunities for better understanding the magnitude of ancient human influence on Amazonia and its current state.

Unraveling Amazon tree community assembly using Maximum Information Entropy: a quantitative analysis of tropical forest ecology.

In a time of rapid global change, the question of what determines patterns in species abundance distribution remains a priority for understanding the complex dynamics of ecosystems. The constrained maximization of information entropy provides a framework for the understanding of such complex systems dynamics by a quantitative analysis of important constraints via predictions using least biased probability distributions. We apply it to over two thousand hectares of Amazonian tree inventories across seven forest types and thirteen functional traits, representing major global axes of plant strategies. Results show that constraints formed by regional relative abundances of genera explain eight times more of local relative abundances than constraints based on directional selection for specific functional traits, although the latter does show clear signals of environmental dependency. These results provide a quantitative insight by inference from large-scale data using cross-disciplinary methods, furthering our understanding of ecological dynamics.