Editorial: Human impacts on bats in tropical ecosystems: sustainable actions and alternatives

Globally, the most extraordinary biodiversity is in the tropics, spread in a great diversity of vegetation types and habitats. Among the myriad mammalian groups, bats stand out for their remarkable taxonomic, functional, and phylogenetic diversity (Wilson and Mittermeier, 2019). Within the tropics, bats can be found in different vegetation types varying in a gradient of structural complexity from dense ancient forests to more open landscapes and woodlands in the savannas and fields (Meyer et al., 2004; Carvalho et al., 2021). Bats provide essential ecosystem services such as seed dispersal and pollination of the many plants that have a role in the income of the most impoverished human populations and the formal economy (Lacher et al., 2019). Moreover, as voracious insect predators, bats play a vital role in suppressing agricultural pests, an invaluable service in this part of the world, and disease vectors for humans (Aguiar et al., 2021; Tuneu-Corral et al., 2023). It is widely recognized that the main threat to bats globally is the extensive conversion of natural ecosystems, especially in tropical developing countries (Meyer et al., 2016). This shift in land use results in habitat loss and environmental degradation, with consequent loss of species, ecosystem services, and lineages (Frick et al., 2020; Atagana et al., 2021; Colombo et al., 2023). There is thus an urgent need to disseminate correct information about bats and explore best practices for mitigating the adverse effects stemming from human activities such as vegetation clearing for cattle ranching, agriculture, human settlements, and urbanization. Therefore, in this Research Topic, we aimed to bring together current research that assesses the influence of multiple environmental transformation drivers on the diversity of tropical bats. Nine papers were published in this Research Topic, and they present novel insights into how bats react to human-driven environmental changes and address significant gaps in bat conservation. These studies were conducted by 36 authors in six countries across the American, African and Asian continents (Figure 1). While the sampling was local in seven studies, Brasileiro et al. used data spanning Brazilian biomes, and Xavier et al. carried out a global systematic review. Three key themes emerge from the papers presented in this Research Topic, and we discuss the findings and knowledge gaps related to each theme in the following sections. Figure 1info:eu-repo/semantics/publishedVersio

Prey preference of the common vampire bat ( Desmodus rotundus

Morphological identification of prey fragments in vampire bat feces is impossible because of an exclusively blood-based diet. Therefore, studies of their foraging ecology require innovative approaches. We investigated the diet of Desmodus rotundus using a PCR-restriction fragment length polymorphism (RFLP) molecular method by amplifying the cytochrome b mitochondrial gene (380 bp) from DNA fecal samples collected from captive bats fed with blood from chickens, cattle, pigs, dogs, and humans - the 5 most frequently attacked prey species in rural areas of the Brazilian Amazonia. The prey preference of the vampire bat was investigated in 18 riverine villages, where the availability of domestic animals to bats was quantified. Prey DNA amplified from fecal samples exhibited no visible signals of vampire bat DNA. A PCR - RFLP flowchart and a combination of 2 DNA restriction enzymes allowed the direct identification of prey to species level. The enzymes' restriction profile did not overlap with those of vampire bats or wild mammal and avian species. Chickens were the most attacked prey species (61.4% of the identifications, n = 27), but pigs were highly preferred in relation to prey availability. This suggests a preference for mammalian blood in D. rotundus diet, with chickens exploited as a secondary food source. No wild vertebrate species was identified in the fecal samples, indicating that vampire bats are selectively feeding on the blood of domesticated animals, probably because they are more predictable and easily accessed resources. © 2015 American Society of Mammalogists

Map of the study area showing the seven sampling modules along the 100-km section of the River Madeira, as follows: TO = Teotônio, MO = Morrinhos, IB = Ilha dos Búfalos, IP = Ilha das Pedras, JL = Jirau Left Bank, JR = Jirau Right Bank, JC = Jaci.

<p>In detail (right), sampling design of each module of 5 km with seven plots (black circles) distributed 50, 500, 1000, 2000, 3000, 4000, and 5000 m from the Rio Madeira bank. All modules were arranged perpendicular to the river.</p

Fear or food? Prey availability is more important than predation risk in determining aerial insectivorous bat responses across a disturbed tropical forest landscape

Habitat disturbance affects, directly or indirectly, the predation risk and food available to animals. One group of animals that may be negatively affected by habitat disturbance are forest-dependent aerial insectivorous bats, especially in the Amazon rainforest, where forest clearance and degradation continue unabated. However, we still have a limited understanding of the mechanisms underlying the negative effect of habitat disturbance on forest aerial insectivorous bats. Evaluating the changes in prey-predator interaction in disturbed habitats can provide helpful information for protected area management. We evaluated how predation risk, insect biomass, and moonlight intensity affect bat activity levels in continuous primary and disturbed forests (fragments and secondary forest) at the Biological Dynamics of Forest Fragments Project, Central Amazon, Brazil. We sampled bats using autonomous ultrasound recorders in continuous forest, forest fragments, and secondary forest. To assess insect biomass, we placed malaise traps close to the recorders and conducted a playback experiment consisting of owl calls to assess the influence of increased predation risk by natural predators on bat activity. We found that continuous forest had higher bat activity than fragments and secondary forest, probably reflecting higher insect biomass in continuous primary forest compared to secondary forest. Insect biomass was the best predictor of activity in disturbed habitats compared to predation risk and moonlight. Predation risk did not modulate bat activity in any habitat type. The effect of moonlight intensity on activity was only apparent in three species in different habitats. Our results suggest that these responses were related to the abundance of specific insect orders and not predation risk. Overall, our findings emphasize the importance of evaluating the effects of prey-predator interactions on the distribution of bats in disturbed tropical forests, as habitat disturbance can negatively affect lower trophic levels and consequently influence not only bats but other insect consumers

Non-metric multidimensional scaling ordination (NMDS) of the bat species composition between sampling plots that were planned to be submerged by the dam (black circles) and those that will remain dry (open circles) at the Santo Antônio hydroelectric power station area, Southwestern Amazonia, Brazil.

<p>Non-metric multidimensional scaling ordination (NMDS) of the bat species composition between sampling plots that were planned to be submerged by the dam (black circles) and those that will remain dry (open circles) at the Santo Antônio hydroelectric power station area, Southwestern Amazonia, Brazil.</p

Establishing baseline biodiversity data prior to hydroelectric dam construction to monitoring impacts to bats in the Brazilian Amazon

<div><p>The modification of Amazonian rivers by the construction of megaprojects of hydroelectric dams has widely increased over the last decade. Robust monitoring programs have been rarely conducted prior to the establishment of dams to measure to what extent the fauna, and its associated habitats may be affected by upcoming impacts. Using bats as models, we performed analyses throughout the area under the influence of the Santo Antônio hydroelectric dam, Southwestern Brazilian Amazonia before its construction to estimate how the fauna and its associated habitats would be affected by the upcoming impacts. We surveyed bats in 49 plots distributed along the areas going to be inundated by the dam and those remaining dry. As predictors for the species distribution, we tested the variables of vegetation structure and topography. Species composition largely differed between the dry plots and the plots located in areas that will be flooded, and this was strongly associated with the variables of forest basal area and elevation. Vegetation-related variables also had strong influence on the guilds distribution. The flooding of lower elevations areas is expected to negatively affect the species number and abundance of frugivorous species. In contrast, it is likely that animalivores will be less vulnerable to dam-induced flooding, since they were abundant in the areas not expect to be inundated. We urge for the implementation of studies to predict impacts caused by large hydroelectric dams, including tests of the influence of the local conditions that shape diversity to avoid massive losses of the biota, and to build preventive monitoring and management actions.</p></div

Relationships between different levels of bat community organization and topographic variables measured in 44 plots along the Madeira River, in Rondônia State, Brazilian Amazonia, between 2010 and 2011.

<p>Partial regression results between elevation and (a) species composition (NMDS axis 2), (b) number of species, and (c) abundance of frugivores. Black circles represent sampling plots that going to be submerged by the dam and white circles represent plots those that will remain dry.</p

Ground-Vegetation Clutter Affects Phyllostomid Bat Assemblage Structure in Lowland Amazonian Forest

<div><p>Vegetation clutter is a limiting factor for bats that forage near ground level, and may determine the distribution of species and guilds. However, many studies that evaluated the effects of vegetation clutter on bats have used qualitative descriptions rather than direct measurements of vegetation density. Moreover, few studies have evaluated the effect of vegetation clutter on a regional scale. Here, we evaluate the influence of the physical obstruction of vegetation on phyllostomid-bat assemblages along a 520 km transect in continuous Amazonian forest. We sampled bats using mist nets in eight localities during 80 nights (3840 net-hours) and estimated the ground-vegetation density with digital photographs. The total number of species, number of animalivorous species, total number of frugivorous species, number of understory frugivorous species, and abundance of canopy frugivorous bats were negatively associated with vegetation clutter. The bat assemblages showed a nested structure in relation to degree of clutter, with animalivorous and understory frugivorous bats distributed throughout the vegetation-clutter gradient, while canopy frugivores were restricted to sites with more open vegetation. The species distribution along the gradient of vegetation clutter was not closely associated with wing morphology, but aspect ratio and wing load differed between frugivores and animalivores. Vegetation structure plays an important role in structuring assemblages of the bats at the regional scale by increasing beta diversity between sites. Differences in foraging strategy and diet of the guilds seem to have contributed more to the spatial distribution of bats than the wing characteristics of the species alone.</p></div

Expected changes in abundance of 48 bat species due to flooding of the Santo Antônio hydroelectric dam, Rondônia State, Brazil, quantified as abundance changes.

<p>Changes of abundance greater than zero indicate species with more captures in plots that going to be submerged by the dam. Black circles: animalivores; white circles: frugivores; grey circles: omnivores; white squares: nectarivores.</p