Secondary forest buffers the effects of fragmentation on aerial insectivorous bat species following 30 years of passive forest restoration

Passive forest restoration can buffer the effects of habitat loss on biodiversity. We acoustically surveyed aerial insectivorous bats in a whole-ecosystem fragmentation experiment in the Brazilian Amazon over a 2-year period, across 33 sites, comprising continuous old-growth forest, remnant fragments, and regenerating secondary forest matrix. We analyzed the activity of 10 species/sonotypes to investigate occupancy across habitat types and responses to fragment size and interior-edge-matrix (IEM) disturbance gradients. Employing a multiscale approach, we investigated guild (edge foragers, forest specialists, flexible forest foragers, and open space specialists) and species-level responses to vegetation structure and forest cover, edge, and patch density across six spatial scales (0.5–3 km). We found species-specific habitat occupancy patterns and nuanced responses to fragment size and the IEM disturbance gradient. For example, Furipterus horrens had lower activity in secondary forest sites and the interior and edge of the smallest fragments (1 and 10 ha) compared to continuous forest, and only two species (Pteronotus spp.) showed no habitat preference and no significant responses across the IEM and fragment size gradients. Only the Molossus sonotype responded negatively to vegetation structure. We uncovered no negative influence of forest cover or edge density at guild or species-level. Our results indicate that reforestation can buffer the negative effects of fragmentation and although these effects can still be detected in some species, generally aerial insectivorous bats appear to be in recovery after 30 years of passive forest restoration. Our findings reinforce the need to protect regenerating forests while conserving vast expanses of old-growth forest

Functional recovery of Amazonian bat assemblages following secondary forest succession

Regenerating forests occupy large areas in the tropics, mostly as a result of deforestation for livestock and agriculture, followed by land abandonment. Despite the importance of regenerating secondary forests for tropical biodiversity conservation, studies of temporal effects of matrix regeneration on species responses in fragmented landscapes are scarce. Here, we used an Amazonian whole-ecosystem fragmentation experiment to investigate how changes in matrix quality over time through secondary forest regeneration affect bat assemblages from a functional perspective. We found that forest regeneration in the matrix positively affected functional α diversity, as well as species- and community-level functional uniqueness, reflecting an increase of species that perform different ecological functions in secondary forest over time. According to functional trait composition, animalivorous species showed the clearest signs of recovery associated with matrix regeneration. Consequently, between-period differences in functional β-diversity were highest in secondary forest compared to fragments and continuous forest, determined mainly by trait gains. However, ~ 30 years of secondary forest regeneration were not sufficient for the functional recovery of bat assemblages to levels observed in continuous forest. Restoring degraded habitats while protecting primary forest will be an important strategy for safeguarding high functional diversity of bats and their vital contributions to ecosystem functioning in fragmented tropical landscapes

The road to functional recovery : temporal effects of matrix regeneration on Amazonian bats

Across the tropics, vast deforested areas are undergoing forest regeneration due to land abandonment. Although secondary forest is an expanding type of landscape matrix that has been shown to buffer some of the negative consequences of forest loss and fragmentation on taxonomic diversity, little is known in this regard about the functional dimension of biodiversity. We took advantage of an ecosystem-wide fragmentation experiment to investigate longer term changes in functional diversity of a mega-diverse Amazonian bat assemblage associated with regrowth development in the matrix. We found that matrix regeneration affected several facets of bat functional diversity in secondary forest over time, increasing functional α diversity, species- and community-level functional uniqueness, altering functional trait composition, and resulting in functional β-diversity changes via trait gains. However, approximately 30 years of matrix regeneration were insufficient for functional diversity to recover to the same levels as in continuous forest. Our results suggest that a combination of natural, human-assisted, and active restoration is likely to be the most successful strategy for restoring functional biodiversity of bats in human-modified tropical landscapes, a finding that most likely also applies to many other taxa

Design matters : an evaluation of the impact of small man-made forest clearings on tropical bats using a before-after-control-impact design

In recent years, large clearings (>1000 ha) accounted for gradually smaller amounts of total annual deforestation in the Brazilian Amazon, whereas the proportion of small clearings (<50 ha) nowadays represents more than 80% of annual deforestation. Despite the ubiquity of small clearings in fragmented Amazonian landscapes, most fragmentation research has focused on the effects of large-scale deforestation, leading to a poor understanding of the impacts of smaller barriers on Amazonian vertebrates. We capitalized on the periodical re-isolation of experimental forest fragments at the Biological Dynamics of Forest Fragments Project in the Central Amazon as a before-after-control-impact experiment to investigate the short-term effects of small clearings on bat assemblages. Over the course of three years we sampled six control sites in continuous forest, the interiors and edges of eight forest fragments as well as eight sites in the surrounding matrix. Sampling took place both before and after the experimental manipulation (clearing of a 100 m wide strip of regrowth around each fragment), resulting in ~4000 bat captures. Species were classified as old-growth specialists and habitat generalists according to their habitat affinities and a joint species distribution modeling framework was used to investigate the effect of fragment re-isolation on species occupancy. Following fragment re-isolation, species richness declined in all habitats other than fragment edges and, although responses were idiosyncratic, this decline was more pronounced for forest specialist than for generalist species. Additionally, fragment re-isolation led to a reduction in the similarity between assemblages in modified habitats (fragment interiors, edges and matrix) and continuous forest. Sampling of controls in continuous forest both prior to and after reisolation revealed that much of the variation in bat species occupancy between sampling periods did not arise from fragment re-isolation but rather reflected natural spatiotemporal variability. This emphasizes the need to sample experimental controls both before and after experimental manipulation and suggests caution in the interpretation of results from studies in which the effects of habitat transformations are assessed based solely on data collected using space-for-time substitution approaches

Design matters : an evaluation of the impact of small man-made forest clearings on tropical bats using a before-after-control-impact design

In recent years, large clearings (>1000 ha) accounted for gradually smaller amounts of total annual deforestation in the Brazilian Amazon, whereas the proportion of small clearings (<50 ha) nowadays represents more than 80% of annual deforestation. Despite the ubiquity of small clearings in fragmented Amazonian landscapes, most fragmentation research has focused on the effects of large-scale deforestation, leading to a poor understanding of the impacts of smaller barriers on Amazonian vertebrates. We capitalized on the periodical re-isolation of experimental forest fragments at the Biological Dynamics of Forest Fragments Project in the Central Amazon as a before-after-control-impact experiment to investigate the short-term effects of small clearings on bat assemblages. Over the course of three years we sampled six control sites in continuous forest, the interiors and edges of eight forest fragments as well as eight sites in the surrounding matrix. Sampling took place both before and after the experimental manipulation (clearing of a 100 m wide strip of regrowth around each fragment), resulting in ~4000 bat captures. Species were classified as old-growth specialists and habitat generalists according to their habitat affinities and a joint species distribution modeling framework was used to investigate the effect of fragment re-isolation on species occupancy. Following fragment re-isolation, species richness declined in all habitats other than fragment edges and, although responses were idiosyncratic, this decline was more pronounced for forest specialist than for generalist species. Additionally, fragment re-isolation led to a reduction in the similarity between assemblages in modified habitats (fragment interiors, edges and matrix) and continuous forest. Sampling of controls in continuous forest both prior to and after reisolation revealed that much of the variation in bat species occupancy between sampling periods did not arise from fragment re-isolation but rather reflected natural spatiotemporal variability. This emphasizes the need to sample experimental controls both before and after experimental manipulation and suggests caution in the interpretation of results from studies in which the effects of habitat transformations are assessed based solely on data collected using space-for-time substitution approaches

Interplay between local and landscape-scale effects on the taxonomic, functional and phylogenetic diversity of aerial insectivorous Neotropical bats

Context Human-modified landscapes are globally ubiquitous. It is critical to understand how habitat loss and fragmentation impact biodiversity from both a local habitat context and landscape-scale perspective to inform land management and conservation strategies. Objectives We used an experimentally fragmented landscape in the Brazilian Amazon to investigate variation in aerial insectivorous bat diversity in response to local habitat and wider landscape characteristics, applying a multiscale approach. Methods We conducted bat acoustic surveys at 33 sites, comprising old secondary forests and fragments of primary forest. Taxonomic, functional and phylogenetic diversity facets were calculated within a Hill numbers framework. We analysed responses to fragment size, interior-edge-matrix gradients, as well as local vegetation structure, continuous forest cover, edge density and patch density across five spatial scales (0.5 km - 3 km) surrounding detector locations. Results Compared with continuous forest, secondary forest matrix around the smallest fragments harboured lower diversity. The overall negative effect of the matrix became less pronounced with increasing fragment size. In contrast, forest edges generally contained higher taxonomic, functional and phylogenetic diversity. We found subtle scale-sensitive associations for FD, responding positively to forest cover (at the 1 km scale) and negatively to edge (1 km scale) and patch density (2.5 km scale). Conclusions Despite a low-contrast matrix of tall secondary forest surrounding fragments after ~30 years of forest recovery, aerial insectivorous bat diversity is not comparable to continuous primary forest. Assemblage functional diversity responds to compositional and configurational landscape characteristics at scales deserving further evaluation at guild and species level

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

Local and Landscape Factors Determining Occurrence of Phyllostomid Bats in Tropical Secondary Forests

Neotropical forests are being increasingly replaced by a mosaic of patches of different successional stages, agricultural fields and pasture lands. Consequently, the identification of factors shaping the performance of taxa in anthropogenic landscapes is gaining importance, especially for taxa playing critical roles in ecosystem functioning. As phyllostomid bats provide important ecological services through seed dispersal, pollination and control of animal populations, in this study we assessed the relationships between phyllostomid occurrence and the variation in local and landscape level habitat attributes caused by disturbance. We mist-netted phyllostomids in 12 sites representing 4 successional stages of a tropical dry forest (initial, early, intermediate and late). We also quantitatively characterized the habitat attributes at the local (vegetation structure complexity) and the landscape level (forest cover, area and diversity of patches). Two focal scales were considered for landscape characterization: 500 and 1000 m. During 142 sampling nights, we captured 606 individuals representing 15 species and 4 broad guilds. Variation in phyllostomid assemblages, ensembles and populations was associated with variation in local and landscape habitat attributes, and this association was scale-dependent. Specifically, we found a marked guild-specific response, where the abundance of nectarivores tended to be negatively associated with the mean area of dry forest patches, while the abundance of frugivores was positively associated with the percentage of riparian forest. These results are explained by the prevalence of chiropterophilic species in the dry forest and of chiropterochorous species in the riparian forest. Our results indicate that different vegetation classes, as well as a multi-spatial scale approach must be considered for evaluating bat response to variation in landscape attributes. Moreover, for the long-term conservation of phyllostomids in anthropogenic landscapes, we must realize that the management of the habitat at the landscape level is as important as the conservation of particular forest fragments