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.

Influence of colony traits on ectoparasite infestation in birds breeding in mixed-species colonies.

Coloniality in birds is often associated with an increase in parasite burden, but whether the co-occurrence of several host species influences the prevalence and abundance of ectoparasites and their relationship with colony size or density remains poorly known. Here, we studied mixed-species breeding colonies formed after the provision of artificial breeding structures for restoring the lesser kestrel (Falco naumanni) population in Portugal, to investigate the influence of colony traits on ectoparasite infestation. We sampled four groups of ectoparasites (carnid flies, haematophagous mites, louse flies and chewing lice) in four hosts: lesser kestrels, European rollers (Coracias garrulus), feral pigeons (Columba livia) and spotless starlings (Sturnus unicolor). Each host species had a distinct infracommunity of ectoparasites, regardless of colony traits such as size, density or host richness. The abundance of the most common ectoparasite, Carnus hemapterus, was influenced by colony composition ­ number of nests of each host species ­ rather than by colony size or density, with its abundance being diluted with increasing numbers of less suitable hosts such as starlings. The increased contact between multiple species of hosts in breeding colonies may complexify host­parasite interactions and challenge our current knowledge on the ecological relationships between host sociality and parasitism.

Changes in grassland management and linear infrastructures associated to the decline of an endangered bird population.

European grassland birds are experiencing major population declines, mainly due to changes in farmland management. We analyzed the role of habitat availability, grazing management and linear infrastructures (roads and power lines) in explaining spatial and temporal variation in the population density of little bustards (Tetrax tetrax) in Portugal, during a decade in which the species population size halved. We used data from 51 areas (totaling ca. 1,50,000 ha) that were sampled in two different periods (2003-2006 and 2016). In 2003-2006, when the species occurred at high densities, habitat availability was the only factor affecting spatial variation in bustard density. In the 2016 survey, variation in density was explained by habitat availability and livestock management, with reduced bird numbers in areas with higher proportions of cattle. Population declines across the study period were steeper in areas that initially held higher densities of bustards and in areas with a higher proportion of cattle in the total stocking rate. Areas with higher densities of power lines also registered greater density declines, probably due to avoidance behavior and to increased mortality. Overall, our results show little bustards are currently lacking high quality grassland habitat, whose persistence depends on extensive grazing regimes and low linear infrastructure densities.

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.

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.

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.

Seasonal variations in the diet and foraging behaviour of dunlins Calidris alpina in a south European estuary: improved feeding conditions for northward migrants.

During the annual cycle, migratory waders may face strikingly different feeding conditions as they move between breeding areas and wintering grounds. Thus, it is of crucial importance that they rapidly adjust their behaviour and diet to benefit from peaks of prey abundance, in particular during migration, when they need to accumulate energy at a fast pace. In this study, we compared foraging behaviour and diet of wintering and northward migrating dunlins in the Tagus estuary, Portugal, by video-recording foraging birds and analysing their droppings. We also estimated energy intake rates and analysed variations in prey availability, including those that were active at the sediment surface. Wintering and northward migrating dunlins showed clearly different foraging behaviour and diet. In winter, birds predominantly adopted a tactile foraging technique (probing), mainly used to search for small buried bivalves, with some visual surface pecking to collect gastropods and crop bivalve siphons. Contrastingly, in spring dunlins generally used a visual foraging strategy, mostly to consume worms, but also bivalve siphons and shrimps. From winter to spring, we found a marked increase both in the biomass of invertebrate prey in the sediment and in the surface activity of worms and siphons. The combination of these two factors, together with the availability of shrimps in spring, most likely explains the changes in the diet and foraging behaviour of dunlins. Northward migrating birds took advantage from the improved feeding conditions in spring, achieving 65% higher energy intake rates as compared with wintering birds. Building on these results and on known daily activity budgets for this species, our results suggest that Tagus estuary provides high-quality feeding conditions for birds during their stopovers, enabling high fattening rates. These findings show that this large wetland plays a key role as a stopover site for migratory waders within the East Atlantic Flyway.

Optimizing sampling design to deal with mist-net avoidance in Amazonian birds and bats.

Mist netting is a widely used technique to sample bird and bat assemblages. However, captures often decline with time because animals learn and avoid the locations of nets. This avoidance or net shyness can substantially decrease sampling efficiency. We quantified the day-to-day decline in captures of Amazonian birds and bats with mist nets set at the same location for four consecutive days. We also evaluated how net avoidance influences the efficiency of surveys under different logistic scenarios using re-sampling techniques. Net avoidance caused substantial declines in bird and bat captures, although more accentuated in the latter. Most of the decline occurred between the first and second days of netting: 28% in birds and 47% in bats. Captures of commoner species were more affected. The numbers of species detected also declined. Moving nets daily to minimize the avoidance effect increased captures by 30% in birds and 70% in bats. However, moving the location of nets may cause a reduction in netting time and captures. When moving the nets caused the loss of one netting day it was no longer advantageous to move the nets frequently. In bird surveys that could even decrease the number of individuals captured and species detected. Net avoidance can greatly affect sampling efficiency but adjustments in survey design can minimize this. Whenever nets can be moved without losing netting time and the objective is to capture many individuals, they should be moved daily. If the main objective is to survey species present then nets should still be moved for bats, but not for birds. However, if relocating nets causes a significant loss of netting time, moving them to reduce effects of shyness will not improve sampling efficiency in either group. Overall, our findings can improve the design of mist netting sampling strategies in other tropical areas.

Latitudinal diversity gradients in New World bats: are they a consequence of niche conservatism?

The increase in species diversity from the Poles to the Equator is a major biogeographic pattern, but the mechanisms underlying it remain obscure. Our aim is to contribute to their clarification by describing the latitudinal gradients in species richness and in evolutionary age of species of New World bats, and testing if those patterns may be explained by the niche conservatism hypothesis. Maps of species ranges were used to estimate species richness in a 100 x 100 km grid. Root distances in a molecular phylogeny were used as a proxy for the age of species, and the mean root distance of the species in each cell of the grid was estimated. Generalised additive models were used to relate latitude with both species richness and mean root distance. This was done for each of the three most specious bat families and for all Chiroptera combined. Species richness increases towards the Equator in the whole of the Chiroptera and in the Phyllostomidae and Molossidae, families that radiated in the tropics, but the opposite trend is observed in the Vespertilionidae, which has a presumed temperate origin. In the whole of the Chiroptera, and in the three main families, there were more basal species in the higher latitudes, and more derived species in tropical areas. In general, our results were not consistent with the predictions of niche conservatism. Tropical niche conservatism seems to keep bat clades of tropical origin from colonizing temperate zones, as they lack adaptations to survive cold winters, such as the capacity to hibernate. However, the lower diversity of Vespertilionidae in the Neotropics is better explained by competition with a diverse pre-existing community of bats than by niche conservatism.

Mosaic-level inference of the impact of land cover changes in agricultural landscapes on biodiversity: a case-study with a threatened grassland bird.

Changes in land use/land cover are a major driver of biodiversity change in the Mediterranean region. Understanding how animal populations respond to these landscape changes often requires using landscape mosaics as the unit of investigation, but few previous studies have measured both response and explanatory variables at the land mosaic level. Here, we used a "whole-landscape" approach to assess the influence of regional variation in the land cover composition of 81 farmland mosaics (mean area of 2900 ha) on the population density of a threatened bird, the little bustard (Tetrax tetrax), in southern Portugal. Results showed that ca. 50% of the regional variability in the density of little bustards could be explained by three variables summarising the land cover composition and diversity in the studied mosaics. Little bustard breeding males attained higher population density in land mosaics with a low land cover diversity, with less forests, and dominated by grasslands. Land mosaic composition gradients showed that agricultural intensification was not reflected in a loss of land cover diversity, as in many other regions of Europe. On the contrary, it led to the introduction of new land cover types in homogenous farmland, which increased land cover diversity but reduced overall landscape suitability for the species. Based on these results, the impact of recent land cover changes in Europe on the little bustard populations is evaluated.

The importance of distance to resources in the spatial modelling of bat foraging habitat.

Many bats are threatened by habitat loss, but opportunities to manage their habitats are now increasing. Success of management depends greatly on the capacity to determine where and how interventions should take place, so models predicting how animals use landscapes are important to plan them. Bats are quite distinctive in the way they use space for foraging because (i) most are colonial central-place foragers and (ii) exploit scattered and distant resources, although this increases flying costs. To evaluate how important distances to resources are in modelling foraging bat habitat suitability, we radio-tracked two cave-dwelling species of conservation concern (Rhinolophus mehelyi and Miniopterus schreibersii) in a Mediterranean landscape. Habitat and distance variables were evaluated using logistic regression modelling. Distance variables greatly increased the performance of models, and distance to roost and to drinking water could alone explain 86 and 73% of the use of space by M. schreibersii and R. mehelyi, respectively. Land-cover and soil productivity also provided a significant contribution to the final models. Habitat suitability maps generated by models with and without distance variables differed substantially, confirming the shortcomings of maps generated without distance variables. Indeed, areas shown as highly suitable in maps generated without distance variables proved poorly suitable when distance variables were also considered. We concluded that distances to resources are determinant in the way bats forage across the landscape, and that using distance variables substantially improves the accuracy of suitability maps generated with spatially explicit models. Consequently, modelling with these variables is important to guide habitat management in bats and similarly mobile animals, particularly if they are central-place foragers or depend on spatially scarce resources.

Structuring of Amazonian bat assemblages: the roles of flooding patterns and floodwater nutrient load.

1. River system dynamics results in ecological heterogeneities that play a central role in maintaining biodiversity in riverine regions. In central Amazonia, large expanses of forest are seasonally flooded by nutrient-rich water (várzea forests) or by nutrient-poor water (igapó forests). Inundation patterns and the nutrient load of floodwaters are perhaps the most important abiotic factors determining spatial ecological variations in lowland Amazonia, and so they are expected to strongly influence the structuring of animal communities. 2. We examined how inundation patterns and water-nutrient load influence the structure of neotropical assemblages of bats, one of the most diverse vertebrate groups in tropical forests. Bat assemblages were sampled with mist nets in central Brazilian Amazonia, across a mosaic of várzea, igapó, and non-flooding nutrient-poor terra firme forests in the low- and high-water seasons. 3. An ordination analysis clearly separated the assemblages of the three forest types, demonstrating the structural relevance of both flooding and floodwater-nutrient load. Flooded forests had lower species richness because of the absence or rarity of species that make roosts out of leaves of understorey plants, and of those that feed on fruits of shrubs. Gleaning insectivores, also partly dependent on the understorey, were less abundant in flooded forests, but aerial insectivores more abundant, presumably because they benefited from a less cluttered foraging environment. These differences suggest that flooding affects bat assemblages mostly because it reduces the availability of niches associated with understorey vegetation, which tends to be sparser in flooded forests. 4. Nutrient-rich várzea forests had a bat biomass twice that of nutrient-poor igapó and unflooded forests. This difference was not only mostly due to a greater overall abundance of bats, but also attributable to a disproportionate higher abundance of large-bodied bat species. 5. We concluded that both flooding and floodwater-nutrient load are very important in the structuring of lowland Amazonian bat assemblages, with inundation mostly constraining the species composition of the assemblages, and water-nutrient load mostly influencing the abundance of species. The distinctiveness of bat assemblages associated with flooding emphasizes the need to preserve inundated forests, which are under particular pressure in Amazonia.

Population structure of a cave-dwelling bat, Miniopterus schreibersii: does it reflect history and social organization?

Many colonial bat species make regional migrations, and the consequent gene flow may eliminate geographic genetic structure resulting from history of colonization. In this study, we verified that history and social organization have detectable impacts on the genetic structure of Miniopterus schreibersii, a cave-dwelling bat with high female philopatry. After studying all known nursing colonies in Portugal, we concluded that there is a significant geographic structure and that the overall pattern is similar for mitochondrial and nuclear DNA. Both pairwise Phi(ST) and F(ST) were significantly correlated with geographical distance, suggesting that isolation by distance is relevant for both mitochondrial and nuclear markers. However, structuring of mitochondrial DNA was much more marked than that of nuclear DNA, a consequence of the strong female philopatry and a bias for male-mediated gene flow. Wintering colonies were more genetically diverse than nursing colonies because the former receive individuals from distinct breeding populations. Haplotype diversity of the northern colonies, the more recent according to population expansion analyses, is only about half of that of the central and southern colonies. This is most likely a consequence of the colonization history of M. schreibersii, which presumably expanded northward from the south of the Iberian Peninsula or North Africa after the last glacial age.

Dispersal of seeds of Hymenaea courbaril (Fabaceae) in a logged rain forest in the Peruvian Amazonian

Foi estudada a dispersão de sementes de Hymenaea courbaril, seguindo o destino de 585 sementes marcadas com imãs e expostas a potenciais dispersores, colocadas em agregados no interior e próximo de uma faixa de floresta cortada, na Amazónia peruana. Mamíferos retiraram frutos de todos os agregados, localizados no interior da floresta, na sua borda, e na clareira. As taxas de remoção foram baixas - mediana de 8.1 frutos/mês em agregados mantidos com 8-10 frutos - mas foram mais altas em agosto que nos primeiros meses do ano. A maior parte dos frutos foi abandonada próxima do agregado de origem ou as suas sementes foram consumidas, mas > 13% foram dispersos com sucesso. A maior parte das sementes dispersas foi enterrada, o que favorece a germinação. A distância máxima de dispersão de sementes vivas foi de 12.1 m (mediana 3.1 m), mas outros imãs foram transportados até 34 m, indicando que as sementes foram dispersas mais longe, mas foram consumidas depois. Cutiaras (muito provavelmente Myoprocta pratti) e cutias (Dasyprocta fuliginosa) parecem ter sido os principais agentes de dispersão. A dispersão de sementes da floresta para o interior da clareira foi rara, sugerindo que apesar de alguns roedores dispersarem H. courbaril, não se pode ficar dependente deles para o repovoamento desta e de outras espécies em clareiras recentes.