Optimizing bat bioacoustic surveys in human-modified Neotropical landscapes.

During the last decades, the use of bioacoustics as a non-invasive and cost-effective sampling method has greatly increased worldwide. For bats, acoustic surveys have long been known to complement traditional mist-netting, however, appropriate protocol guidelines are still lacking for tropical regions. Establishing the minimum sampling effort needed to detect ecological changes in bat assemblages (e.g., activity, composition, and richness) is crucial in view of workload and project cost constraints, and because detecting such changes must be reliable enough to support effective conservation management. Using one of the most comprehensive tropical bat acoustic data sets, collected in the Amazon, we assessed the minimum survey effort required to accurately assess the completeness of assemblage inventories and habitat selection in fragmented forest landscapes for aerial insectivorous bats. We evaluated a combination of 20 different temporal sampling schemes, which differed regarding number of hours per night, number of nights per site, and sampling only during the wet or dry season, or both. This was assessed under two different landscape scenarios: in primary forest fragments embedded in a matrix of secondary forest and in the same forest fragments, but after they had been re-isolated through clearing of the secondary forest. We found that the sampling effort required to achieve 90% inventory completeness varied considerably depending on the research aim and the landscape scenario evaluated, averaging ~80 and 10 nights before and after fragment re-isolation, respectively. Recording for more than 4 h per night did not result in a substantial reduction in the required number of sampling nights. Regarding the effects of habitat selection, except for assemblage composition, bat responses in terms of richness, diversity, and activity were similar across all sampling schemes after fragment re-isolation. However, before re-isolation, a minimum of four to six sampling hours per night after dusk and three to five nights of sampling per site were needed to detect significant effects that could otherwise go unnoticed. Based on our results, we propose guidelines that will aid to optimize sampling protocols for bat acoustic surveys in the Neotropics.

Predicting biodiversity change and averting collapse in agricultural landscapes.

The equilibrium theory of island biogeography is the basis for estimating extinction rates and a pillar of conservation science. The default strategy for conserving biodiversity is the designation of nature reserves, treated as islands in an inhospitable sea of human activity. Despite the profound influence of islands on conservation theory and practice, their mainland analogues, forest fragments in human-dominated landscapes, consistently defy expected biodiversity patterns based on island biogeography theory. Countryside biogeography is an alternative framework, which recognizes that the fate of the world's wildlife will be decided largely by the hospitality of agricultural or countryside ecosystems. Here we directly test these biogeographic theories by comparing a Neotropical countryside ecosystem with a nearby island ecosystem, and show that each supports similar bat biodiversity in fundamentally different ways. The island ecosystem conforms to island biogeographic predictions of bat species loss, in which the water matrix is not habitat. In contrast, the countryside ecosystem has high species richness and evenness across forest reserves and smaller forest fragments. Relative to forest reserves and fragments, deforested countryside habitat supports a less species-rich, yet equally even, bat assemblage. Moreover, the bat assemblage associated with deforested habitat is compositionally novel because of predictable changes in abundances by many species using human-made habitat. Finally, we perform a global meta-analysis of bat biogeographic studies, spanning more than 700 species. It generalizes our findings, showing that separate biogeographic theories for countryside and island ecosystems are necessary. A theory of countryside biogeography is essential to conservation strategy in the agricultural ecosystems that comprise roughly half of the global land surface and are likely to increase even further.

A global risk assessment of primates under climate and land use/cover scenarios.

Primates are facing an impending extinction crisis, driven by extensive habitat loss, land use change and hunting. Climate change is an additional threat, which alone or in combination with other drivers, may severely impact those taxa unable to track suitable environmental conditions. Here, we investigate the extent of climate and land use/cover (LUC) change-related risks for primates. We employed an analytical approach to objectively select a subset of climate scenarios, for which we then calculated changes in climatic and LUC conditions for 2050 across primate ranges (N = 426 species) under a best-case scenario and a worst-case scenario. Generalized linear models were used to examine whether these changes varied according to region, conservation status, range extent and dominant habitat. Finally, we reclassified primate ranges based on different magnitudes of maximum temperature change, and quantified the proportion of ranges overall and of primate hotspots in particular that are likely to be exposed to extreme temperature increases. We found that, under the worst-case scenario, 74% of Neotropical forest-dwelling primates are likely to be exposed to maximum temperature increases up to 7°C. In contrast, 38% of Malagasy savanna primates will experience less pronounced warming of up to 3.5°C. About one quarter of Asian and African primates will face up to 50% crop expansion within their range. Primary land (undisturbed habitat) is expected to disappear across species' ranges, whereas secondary land (disturbed habitat) will increase by up to 98%. With 86% of primate ranges likely to be exposed to maximum temperature increases >3°C, primate hotspots in the Neotropics are expected to be particularly vulnerable. Our study highlights the fundamental exposure risk of a large percentage of primate ranges to predicted climate and LUC changes. Importantly, our findings underscore the urgency with which climate change mitigation measures need to be implemented to avert primate extinctions on an unprecedented scale.

Species undersampling in tropical bat surveys: effects on emerging biodiversity patterns.

Undersampling is commonplace in biodiversity surveys of species-rich tropical assemblages in which rare taxa abound, with possible repercussions for our ability to implement surveys and monitoring programmes in a cost-effective way. We investigated the consequences of information loss due to species undersampling (missing subsets of species from the full species pool) in tropical bat surveys for the emerging patterns of species richness (SR) and compositional variation across sites. For 27 bat assemblage data sets from across the tropics, we used correlations between original data sets and subsets with different numbers of species deleted either at random, or according to their rarity in the assemblage, to assess to what extent patterns in SR and composition in data subsets are congruent with those in the initial data set. We then examined to what degree high sample representativeness (r ≥ 0·8) was influenced by biogeographic region, sampling method, sampling effort or structural assemblage characteristics. For SR, correlations between random subsets and original data sets were strong (r ≥ 0·8) with moderate (ca. 20%) species loss. Bias associated with information loss was greater for species composition; on average ca. 90% of species in random subsets had to be retained to adequately capture among-site variation. For nonrandom subsets, removing only the rarest species (on average c. 10% of the full data set) yielded strong correlations (r > 0·95) for both SR and composition. Eliminating greater proportions of rare species resulted in weaker correlations and large variation in the magnitude of observed correlations among data sets. Species subsets that comprised ca. 85% of the original set can be considered reliable surrogates, capable of adequately revealing patterns of SR and temporal or spatial turnover in many tropical bat assemblages. Our analyses thus demonstrate the potential as well as limitations for reducing survey effort and streamlining sampling protocols, and consequently for increasing the cost-effectiveness in tropical bat surveys or monitoring programmes. The dependence of the performance of species subsets on structural assemblage characteristics (total assemblage abundance, proportion of rare species), however, underscores the importance of adaptive monitoring schemes and of establishing surrogate performance on a site by site basis based on pilot surveys.

Where to nest? Ecological determinants of chimpanzee nest abundance and distribution at the habitat and tree species scale.

Conversion of forests to anthropogenic land-uses increasingly subjects chimpanzee populations to habitat changes and concomitant alterations in the plant resources available to them for nesting and feeding. Based on nest count surveys conducted during the dry season, we investigated nest tree species selection and the effect of vegetation attributes on nest abundance of the western chimpanzee, Pan troglodytes verus, at Lagoas de Cufada Natural Park (LCNP), Guinea-Bissau, a forest-savannah mosaic widely disturbed by humans. Further, we assessed patterns of nest height distribution to determine support for the anti-predator hypothesis. A zero-altered generalized linear mixed model showed that nest abundance was negatively related to floristic diversity (exponential form of the Shannon index) and positively with the availability of smaller-sized trees, reflecting characteristics of dense-canopy forest. A positive correlation between nest abundance and floristic richness (number of plant species) and composition indicated that species-rich open habitats are also important in nest site selection. Restricting this analysis to feeding trees, nest abundance was again positively associated with the availability of smaller-sized trees, further supporting the preference for nesting in food tree species from dense forest. Nest tree species selection was non-random, and oil palms were used at a much lower proportion (10%) than previously reported from other study sites in forest-savannah mosaics. While this study suggests that human disturbance may underlie the exclusive arboreal nesting at LCNP, better quantitative data are needed to determine to what extent the construction of elevated nests is in fact a response to predators able to climb trees. Given the importance of LCNP as refuge for Pan t. verus our findings can improve conservation decisions for the management of this important umbrella species as well as its remaining suitable habitats.

Edge effects and vertical stratification of aerial insectivorous bats across the interface of primary-secondary Amazonian rainforest.

Edge effects, abiotic and biotic changes associated with habitat boundaries, are key drivers of community change in fragmented landscapes. Their influence is heavily modulated by matrix composition. With over half of the world's tropical forests predicted to become forest edge by the end of the century, it is paramount that conservationists gain a better understanding of how tropical biota is impacted by edge gradients. Bats comprise a large fraction of tropical mammalian fauna and are demonstrably sensitive to habitat modification. Yet, knowledge about how bat assemblages are affected by edge effects remains scarce. Capitalizing on a whole-ecosystem manipulation in the Central Amazon, the aims of this study were to i) assess the consequences of edge effects for twelve aerial insectivorous bat species across the interface of primary and secondary forest, and ii) investigate if the activity levels of these species differed between the understory and canopy and if they were modulated by distance from the edge. Acoustic surveys were conducted along four 2-km transects, each traversing equal parts of primary and ca. 30-year-old secondary forest. Five models were used to assess the changes in the relative activity of forest specialists (three species), flexible forest foragers (three species), and edge foragers (six species). Modelling results revealed limited evidence of edge effects, except for forest specialists in the understory. No significant differences in activity were found between the secondary or primary forest but almost all species exhibited pronounced vertical stratification. Previously defined bat guilds appear to hold here as our study highlights that forest bats are more edge-sensitive than edge foraging bats. The absence of pronounced edge effects and the comparable activity levels between primary and old secondary forests indicates that old secondary forest can help ameliorate the consequences of fragmentation on tropical aerial insectivorous bats.

Second-growth and small forest clearings have little effect on the temporal activity patterns of Amazonian phyllostomid bats.

Secondary forests and human-made forest gaps are conspicuous features of tropical landscapes. Yet, behavioral responses to these aspects of anthropogenically modified forests remain poorly investigated. Here, we analyze the effects of small human-made clearings and secondary forests on tropical bats by examining the guild- and species-level activity patterns of phyllostomids sampled in the Central Amazon, Brazil. Specifically, we contrast the temporal activity patterns and degree of temporal overlap of 6 frugivorous and 4 gleaning animalivorous species in old-growth forest and second-growth forest and of 4 frugivores in old-growth forest and forest clearings. The activity patterns of frugivores and gleaning animalivores did not change between old-growth forest and second-growth, nor did the activity patterns of frugivores between old-growth forest and clearings. However, at the species level, we detected significant differences for Artibeus obscurus (old-growth forest vs. second-growth) and A. concolor (old-growth forest vs. clearings). The degree of temporal overlap was greater than random in all sampled habitats. However, for frugivorous species, the degree of temporal overlap was similar between old-growth forest and second-growth; whereas for gleaning animalivores, it was lower in second-growth than in old-growth forest. On the contrary, forest clearings were characterized by increased temporal overlap between frugivores. Changes in activity patterns and temporal overlap may result from differential foraging opportunities and dissimilar predation risks. Yet, our analyses suggest that activity patterns of bats in second-growth and small forest clearings, 2 of the most prominent habitats in humanized tropical landscapes, varies little from the activity patterns in old-growth forest.

Author Correction: A global database for metacommunity ecology, integrating species, traits, environment and space.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A global database for metacommunity ecology, integrating species, traits, environment and space.

The use of functional information in the form of species traits plays an important role in explaining biodiversity patterns and responses to environmental changes. Although relationships between species composition, their traits, and the environment have been extensively studied on a case-by-case basis, results are variable, and it remains unclear how generalizable these relationships are across ecosystems, taxa and spatial scales. To address this gap, we collated 80 datasets from trait-based studies into a global database for metaCommunity Ecology: Species, Traits, Environment and Space; "CESTES". Each dataset includes four matrices: species community abundances or presences/absences across multiple sites, species trait information, environmental variables and spatial coordinates of the sampling sites. The CESTES database is a live database: it will be maintained and expanded in the future as new datasets become available. By its harmonized structure, and the diversity of ecosystem types, taxonomic groups, and spatial scales it covers, the CESTES database provides an important opportunity for synthetic trait-based research in community ecology.

Quantifying and addressing the prevalence and bias of study designs in the environmental and social sciences.

Building trust in science and evidence-based decision-making depends heavily on the credibility of studies and their findings. Researchers employ many different study designs that vary in their risk of bias to evaluate the true effect of interventions or impacts. Here, we empirically quantify, on a large scale, the prevalence of different study designs and the magnitude of bias in their estimates. Randomised designs and controlled observational designs with pre-intervention sampling were used by just 23% of intervention studies in biodiversity conservation, and 36% of intervention studies in social science. We demonstrate, through pairwise within-study comparisons across 49 environmental datasets, that these types of designs usually give less biased estimates than simpler observational designs. We propose a model-based approach to combine study estimates that may suffer from different levels of study design bias, discuss the implications for evidence synthesis, and how to facilitate the use of more credible study designs.

FragSAD: A database of diversity and species abundance distributions from habitat fragments.

Habitat destruction is the single greatest anthropogenic threat to biodiversity. Decades of research on this issue have led to the accumulation of hundreds of data sets comparing species assemblages in larger, intact, habitats to smaller, more fragmented, habitats. Despite this, little synthesis or consensus has been achieved, primarily because of non-standardized sampling methodology and analyses of notoriously scale-dependent response variables (i.e., species richness). To be able to compare and contrast the results of habitat fragmentation on species' assemblages, it is necessary to have the underlying data on species abundances and sampling intensity, so that standardization can be achieved. To accomplish this, we systematically searched the literature for studies where abundances of species in assemblages (of any taxa) were sampled from many habitat patches that varied in size. From these, we extracted data from several studies, and contacted authors of studies where appropriate data were collected but not published, giving us 117 studies that compared species assemblages among habitat fragments that varied in area. Less than one-half (41) of studies came from tropical forests of Central and South America, but there were many studies from temperate forests and grasslands from all continents except Antarctica. Fifty-four of the studies were on invertebrates (mostly insects), but there were several studies on plants (15), birds (16), mammals (19), and reptiles and amphibians (13). We also collected qualitative information on the length of time since fragmentation. With data on total and relative abundances (and identities) of species, sampling effort, and affiliated meta-data about the study sites, these data can be used to more definitively test hypotheses about the role of habitat fragmentation in altering patterns of biodiversity. There are no copyright restrictions. Please cite this data paper and the associated Dryad data set if the data are used in publications.

Secondary forest regeneration benefits old-growth specialist bats in a fragmented tropical landscape.

Tropical forest loss and fragmentation are due to increase in coming decades. Understanding how matrix dynamics, especially secondary forest regrowth, can lessen fragmentation impacts is key to understanding species persistence in modified landscapes. Here, we use a whole-ecosystem fragmentation experiment to investigate how bat assemblages are influenced by the regeneration of the secondary forest matrix. We surveyed bats in continuous forest, forest fragments and secondary forest matrix habitats, ~15 and ~30 years after forest clearance, to investigate temporal changes in the occupancy and abundance of old-growth specialist and habitat generalist species. The regeneration of the second growth matrix had overall positive effects on the occupancy and abundance of specialists across all sampled habitats. Conversely, effects on generalist species were negligible for forest fragments and negative for secondary forest. Our results show that the conservation potential of secondary forests for reverting faunal declines in fragmented tropical landscapes increases with secondary forest age and that old-growth specialists, which are often of most conservation concern, are the greatest beneficiaries of secondary forest maturation. Our findings emphasize that the transposition of patterns of biodiversity persistence in island ecosystems to fragmented terrestrial settings can be hampered by the dynamic nature of human-dominated landscapes.

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

We synthesize findings from one of the world's 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. Even within our controlled study area, the landscape has been highly dynamic: for example, the matrix of vegetation surrounding fragments has changed markedly over time, succeeding from large cattle pastures or forest clearcuts to secondary regrowth forest. This, in turn, has influenced the dynamics of plant and animal communities and their trajectories of change over time. In general, fauna and flora have responded differently to fragmentation: the most locally extinction-prone animal species are those that have both large area requirements and low tolerance of the modified habitats surrounding fragments, whereas the most vulnerable plants are those that respond poorly to edge effects or chronic forest disturbances, and that rely on vulnerable animals for seed dispersal or pollination. Relative to intact forests, most fragments are hyperdynamic, with unstable or fluctuating populations of species in response to a variety of external vicissitudes. Rare weather events such as droughts, windstorms and floods have had strong impacts on fragments and left lasting legacies of change. Both forest fragments and the intact forests in our study area appear to be influenced by larger-scale environmental drivers operating at regional or global scales. These drivers are apparently increasing forest productivity and have led to concerted, widespread increases in forest dynamics and plant growth, shifts in tree-community composition, and increases in liana (woody vine) abundance. Such large-scale drivers are likely to interact synergistically with habitat fragmentation, exacerbating its effects for some species and ecological phenomena. Hence, the impacts of fragmentation on Amazonian biodiversity and ecosystem processes appear to be a consequence not only of local site features but also of broader changes occurring at landscape, regional and even global scales.

Season-modulated responses of Neotropical bats to forest fragmentation.

Seasonality causes fluctuations in resource availability, affecting the presence and abundance of animal species. The impacts of these oscillations on wildlife populations can be exacerbated by habitat fragmentation. We assessed differences in bat species abundance between the wet and dry season in a fragmented landscape in the Central Amazon characterized by primary forest fragments embedded in a secondary forest matrix. We also evaluated whether the relative importance of local vegetation structure versus landscape characteristics (composition and configuration) in shaping bat abundance patterns varied between seasons. Our working hypotheses were that abundance responses are species as well as season specific, and that in the wet season, local vegetation structure is a stronger determinant of bat abundance than landscape-scale attributes. Generalized linear mixed-effects models in combination with hierarchical partitioning revealed that relationships between species abundances and local vegetation structure and landscape characteristics were both season specific and scale dependent. Overall, landscape characteristics were more important than local vegetation characteristics, suggesting that landscape structure is likely to play an even more important role in landscapes with higher fragment-matrix contrast. Responses varied between frugivores and animalivores. In the dry season, frugivores responded more to compositional metrics, whereas during the wet season, local and configurational metrics were more important. Animalivores showed similar patterns in both seasons, responding to the same group of metrics in both seasons. Differences in responses likely reflect seasonal differences in the phenology of flowering and fruiting between primary and secondary forests, which affected the foraging behavior and habitat use of bats. Management actions should encompass multiscale approaches to account for the idiosyncratic responses of species to seasonal variation in resource abundance and consequently to local and landscape scale attributes.

Dispersal and group formation dynamics in a rare and endangered temperate forest bat (Nyctalus lasiopterus, Chiroptera: Vespertilionidae).

For elusive mammals like bats, colonization of new areas and colony formation are poorly understood, as is their relationship with the genetic structure of populations. Understanding dispersal and group formation behaviors is critical not only for a better comprehension of mammalian social dynamics, but also for guiding conservation efforts of rare and endangered species. Using nuclear and mitochondrial markers, we studied patterns of genetic diversity and differentiation among and within breeding colonies of giant noctule bats (Nyctalus lasiopterus), their relation to a new colony still in formation, and the impact of this ongoing process on the regionwide genetic makeup. Nuclear differentiation among colonies was relatively low and mostly nonsignificant. Mitochondrial variation followed this pattern, contrasting with findings for other temperate bat species. Our results suggest that this may indicate a recent population expansion. On average, female giant noctules were not more closely related to other colony members than to foreign individuals. This was also true for members of the newly forming colony and those of another, older group sampled shortly after its formation, suggesting that contrary to findings for other temperate bats, giant noctule colonies are not founded by relatives. However, mother-daughter pairs were found in the same populations more often than expected under random dispersal. Given this indication of philopatry, the lack of mitochondrial differentiation among most colonies in the region is probably due to the combination of a recent population expansion and group formation events.

Flying high--assessing the use of the aerosphere by bats.

Bats feature prominently among organisms that occupy the aerosphere as they extensively use this environment for foraging, but also for dispersal, migration, and behavioral interactions. Differential use of the aerosphere is an important factor structuring bat assemblages, with species exhibiting distinct morphological, physiological, and sensory adaptations to different habitat types. This necessitates comprehensive sampling methodologies such as combined ground-level and canopy-level mist netting as well as acoustic monitoring to assess the presence, diversity, and activity of different functional groups of species adequately. Recent technological advances in acoustic detection and in methods of analysis, coupled with the expansion of libraries of echolocation calls for species identification, now allow for the reliable quantification of species numbers and activity of the scarcely known group of aerial insectivorous bats, particularly in species-rich tropical assemblages. We provide a brief, exemplary overview of recent studies on bats conducted in Panamá to demonstrate the necessity of comprehensive sampling methods and application of new technologies in order to adequately depict assemblage composition and responses of bats to structural changes in habitats induced by fragmentation. In addition to acoustic methods, miniaturization of radio transmitters has provided new insights into the patterns of spatial use of the aerosphere by bats and has identified species-specific differences in mobility as one of the important traits that determines bats' reactions to anthropogenic alterations of the landscape. Following the goals of the symposium on aeroecology, we propose new avenues of research for probing the aerosphere. We discuss how integration of a diverse array of remote sensing tools with data on species distribution and species traits, such as mobility and edge-sensitivity, might provide novel opportunities for the development, and application of conservation-oriented monitoring systems.