Maria João Ramos Pereira

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.

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.

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.

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.

Behavioural determinants of gene flow in the bat Miniopterus schreibersii

Dispersal and migratory behaviours are often important determinants of gene flow in wild species, and we have studied their role using ringing-recapture data in the Portuguese population of Miniopterus schreibersii, a cave-dwelling bat that forms large maternity colonies. Juvenile dispersal, usually a major agent of gene flow, appears to be negligible, as young females never settled to give birth in foreign colonies. Likewise, there was virtually no dispersal of adult females to foreign maternity colonies. This strong philopatry virtually eliminated female-mediated gene flow, but we found a great potential for male-mediated gene flow among colonies, as regional migrations temporarily joined both sexes from different colonies in the same roosts, during the mating season. In fact, females from some colonies were more likely to mate with males from foreign colonies than from their own, thus potentially bringing home genes of foreign males. In spite of this abundant gene flow, we found a pattern of isolation by distance and even strong barriers to gene flow, which is explained by the fact that migrations were usually too short to allow direct flow among distant colonies. We concluded that potential gene flow is influenced by the distance between colonies and the availability of mating roosts between them. In addition, we found this flow to be asymmetrical, with a dominant direction from the largest to the smallest colonies. Our ringing-recapture estimates of potential gene flow based on dispersal and migratory behaviour are compatible with the genetic structure of the population for both nuclear and mitochondrial DNA. Our conclusions have implications for the conservation of bats with a spatial behaviour similar to that of M. schreibersii. Colonies should be managed individually because strict female philopatry not only promotes their isolation but also minimises the contribution of immigration in rescuing declining colonies. Furthermore, the results underline the importance of preserving mating roosts to maintain gene flow among colonies.

MARGOV – building social sustainability

Structured in three components Governance, Citizenship and Dynamic-Spatial Structure – the MARGov project aims to build a Model of Collaborative Governance for Marine Protected Areas using as case study the Marine Park Professor Luiz Saldanha. The objective is to empower local communities enabling them to be agents for change for the sustainable governance of the Ocean, through an eco-social dialogue supported by active participation. This intends to reinforce competences and the co-responsibility of all the actors involved. In this paper the authors present the work developed in the first component – Governance – essential to assure social sustainability. A successful Marine Protected Area strongly depends on the balance between man and environment, and therefore, on the eco-social dialogue that is possible to be established among all actors. According to the literature, the building up of participatory formats that assure the articulation between different groups, enhancing the constructive dialogue aiming at achieving sustainable management, contributes to the overlay of knowledge and different perspectives, and generates enriched and more robust solutions. It also says that such processes generate new synergies and potentiate the exchange of ideas, experiences, technical-scientific cooperation, as well as the integration of knowledge and good practices, and that they frequently create the conditions for the emergence of innovative alternatives. This paper is about the participatory sessions created and conducted as part of the Governance component of the project, describing the methodology developed for the expanded involvement of local communities aiming at building a model of Collaborative Governance. It also presents the strategy developed by the MARGov team to reinforce the social component, through continuous improvement of a communication strategy and the setting up of a constructive participatory process. Finally, it presents the results of the dialog generated in these fora and it discusses all this in the context of a general conceptual framework. It also identifies what made an actual difference, and the lessons learned, theorizing from action and exploring how to pursue.

Following The Trail: Factors Underlying the Sudden Expansion of the Egyptian Mongoose ( Herpestes ichneumon ) in Portugal

Species range-limits are influenced by a combination of several factors. In our study we aimed to unveil the drivers underlying the expansion of the Egyptian mongoose in Portugal, a carnivore that was confined to southern Portugal and largely increased its range during the last three decades. We evaluated the expansion of the species in three periods (1980-1990, 1990-2000 and 2000-2010), by projecting the presence/absence data of the species in each temporal range and proposed four hypotheses to explain this sudden expansion associated to changes in the barrier effects of human infrastructure and topographic features, and in the availability of suitable areas due to climate change or land use. An exploratory analysis was made using Spearman rank correlation, followed by a hierarchical partitioning analysis to select uncorrelated potential explanatory variables associated with the different hypotheses. We then ran Generalized Linear Models (GLM) for every period for each hypothesis and for every combination of hypotheses. Our main findings suggest that dynamic transitions of land-use coupled with temperature and rainfall variations over the decades are the main drivers promoting the mongoose expansion. The geographic barriers and the human infrastructures functioned as barriers for mongoose expansion and have shaped its distribution. The expansion of the Egyptian mongoose across the Portuguese territory was due to a variety of factors. Our results suggest a rapid shift in species range in response to land-use and climate changes, underlining the close link between species ranges and a changing environment.

A mosaic of opportunities? Spatio-temporal patterns of bat diversity and activity in a strongly humanized Mediterranean wetland

The Baixo Vouga Lagunar (BVL) landscape, in the Portuguese central-west coast, harbours a mosaic of wetland habitat types, interspersed by intensive and extensive agricultural fields, pastures, production forests and urban areas. In this study, we aimed to determine the species composition and the structure of the bat assemblages of the different habitats that constitute this heterogeneous landscape and to investigate seasonal changes in the patterns of bat diversity and activity across habitats. We acoustically sampled bats across 24 sampling sites representative of the eight main habitat types that shape the landscape—Bocage, forests, maize fields, marshlands, reed beds, rice fields, sea rushes and urban settlements. We compared bat richness, diversity and evenness across habitat types and seasons. We analysed habitat-specific and season-specific overall bat activity, and because habitat selection by bats is known to reflect morphological characters, foraging strategies and echolocation call structures, we also analysed the activity of individual species and of eco-morphological guilds. From 1,544 bat-passes recorded, we identified 12 species. Pipistrellus pygmaeus, Pipistrellus pipistrellus and Eptesicus serotinus/Eptesicus isabellinus were the most frequently recorded. Species composition and activity were similar across habitats, whilst exhibiting strong seasonal dynamics within habitats. Our results suggest that the mosaicism of the landscape provides several opportunities for bats, enabling them to explore different resources in distinct habitat patches. However, it may also reflect a forced exploitation of less optimal habitats and resources by bats, due to the scarcity of opportunities provided by fragmented landscapes.

Availability of Food for Frugivorous Bats in Lowland Amazonia: The Influence of Flooding and of River Banks

In Neotropical forests fruits are key resources for a great diversity of vertebrates, including many frugivorous bats, but little is known about the factors that determine their availability. We studied forest inundation and river banks as determinants of the spatial variation in the availability of fruits for bats in lowland Amazonia. We sampled the bat assemblage composition, fruit availability, and bat diet in terra firme upland forest and in two types of flooded forest — várzea and igapó. Two distinct frugivore bat guilds were found in both terra firme and flooded forests: (1) canopy frugivores, feeding mainly on Ficus and Cecropia, and (2) understorey frugivores that feed mainly on Vismia and Piper. Fruits consumed by the canopy guild were more abundant in the flooded forests — particularly in the nutrient-rich várzea, but those dominating the understory guild diet were most abundant in terra firme. Availability of both fruit genera most consumed by the canopy guild was greater along river banks than in the forest matrix. For the understory guild, the greater abundance of Vismia along river banks was compensated for by a higher availability of Piper in the matrix. In conclusion, both factors influence the availability of fruits, although differently for the canopy and understory guilds. The resulting differences in fruit abundance may explain variations in bat assemblages of the different forest types. River banks play a particularly important role in providing food for bats of both guilds, but are under particularly heavy human pressure.

Bat richness and activity in heterogeneous landscapes: guild-specific and scale-dependent?

ContextThe conversion of natural environments into agricultural land has profound effects on the composition of the landscape, often resulting in a mosaic of human-altered and natural habitats. The response to these changes may however vary among organisms. Bats are highly vagile, and their requirements often imply the use of distinct habitats, which they select responding to both landscape and local features.ObjectivesWe aimed to identify which features influence bat richness and activity within Baixo Vouga Lagunar, a heterogeneous landscape located on the Central-North Portuguese coast, and to investigate if that influence varies across a gradient of focal scales.MethodsWe sampled bats acoustically, while simultaneously sampling insects with light traps. We assessed the relationships between species richness, bat activity, and activity of eco-morphological guilds with landscape and local features, across four scales.ResultsOur results revealed both scale- and guild-dependent responses of bats to landscape and local features. At broader scales we found positive associations between open-space foraging bats and habitat heterogeneity and between edge-space foraging bats and greater edge lengths. Woodland cover and water availability at an intermediate scale and weather conditions and insect abundance at a local scale were the factors that mostly influenced the response variables.ConclusionsGlobally, our results suggest that bats are sensitive to local resource availability and distribution, while simultaneously reacting to landscape features acting at coarser scales. Finally, our results suggest that the responses given by bats are guild-dependent, and some habitats act as keystone structures for bats within this mosaic.