Ecology and conservation of insectivorous bats in rural landscapes

Throughout the world, the increasing use of land for agriculture has been associated with extensive loss and fragmentation of natural habitats and, frequently, the degradation of remaining habitats. The effects of such habitat changes have been well studied for some faunal groups, but little is known of their consequences for bats. The aim of this study was to investigate the ecology and conservation of an assemblage of insectivorous bats in a rural landscape, with particular focus on their foraging and roosting requirements. This increased knowledge will, hopefully, assist the formulation of policy and management decisions to ensure the long-term survival of bats in these altered environments. The distribution and abundance of insectivorous bats in the Northern Plains of Victoria was investigated to determine the impacts of land-use change and to identify factors influencing the distribution of bats in rural landscapes. Thirteen species of insectivorous bats were recorded across the region by sampling at 184 sites. Two species were rare, but the remaining 11 species were widespread and occurred in all types of remnant wooded vegetation, ranging from large blocks (≥200 ha) to small isolated remnants (≤5 ha) and scattered trees in cleared farm paddocks. There was no significant difference between remnant types in the relative abundance of bat species, in species richness, or in the composition of bat assemblages at study sites. In a subsequent study, no difference in the activity levels of bats was found between remnants with different tree densities, ranging from densely-vegetated blocks to single paddock trees. However, sites in open paddocks devoid of trees differed significantly from all types of wooded remnants and had significantly lower levels of bat activity and a different species composition. In highly cleared and modified landscapes, all native vegetation has value to bats, even the smallest remnant, roadside and single paddock tree. Roost sites are a key habitat requirement for bats and may be a limiting resource in highly modified environments. Two species, the lesser long-eared bat Nyctophilus geoffroyi and Gould's wattled bat Chalinolobus gouldii, were investigated as a basis for understanding the capacity of bats to survive in agricultural landscapes. These species have different wing morphologies, which may be influential in how they use the landscape, and anecdotal evidence suggested differences in their roosting ecology. Roosting ecology was examined using radio-tracking to locate 376 roosts in two study areas with contrasting tree cover in northern Victoria. Both species were highly selective in the location of their roosts in the landscape, in roost-site selection and in roosting behaviour, and responded differently to differing levels of availability of roosts. The Barmah-Picola study area incorporated remnant vegetation in farmland and an adjacent extensive floodplain forest (Barmah forest). Male N. geojfroyi roosted predominantly within 3 km of their foraging areas in remnants in farmland. However, most female N. geoffroyi, and both sexes of C. gouldii, roosted in Barmah forest up to 12 km from their foraging areas in farmland remnants. These distances were greater than previously recorded for these species and further than predicted by wing morphology. In contrast, in the second study area (Naring) where only small remnants of wooded vegetation remain in farmland, individuals of both species moved significantly shorter distances between roost sites and foraging areas. There were marked inter- and intra-specific differences in the roosts selected. C. gouldii used similar types of roosts in both areas - predominantly dead spouts in large, live trees. N. geoffroyi used a broader range of roost types, especially in the farmland environment. Roosts were typically under bark and in fissures, with males in particular also using anthropogenic structures. A strong preference was shown by both sexes for roosts in dead trees, and entrance dimensions of roosts were consistently narrow (2.5 cm). In Barmah forest, maternity roosts used by N. geoffroyi were predominantly in narrow fissures in large-diameter, dead trees, while at Naring maternity roosts were also found under bark, in buildings, and in small-diameter, live and dead trees. The number of roost trees that are required for an individual or colony is influenced by the frequency with which bats move between roosts, the proportion of roosts that are re-used, the distance between consecutive roosts, and the size of roosting colonies. Both species roosted in small colonies and regularly shifted roost sites within a discrete roost area. These behavioural traits suggest that a high density of roost sites is required. There were marked differences in these aspects of behaviour between individuals roosting in Barmah forest and in the fragmented rural landscape. At Naring, N. geqffroyi remained in roosts for longer periods and moved greater distances between consecutive roosts than in Barmah forest. In contrast, C. gouldii used a smaller pool of roosts in the farmland environment by re-using roosts more frequently. Within Barmah forest, there is an extensive area of forest but the density of hollow-bearing trees is reduced due to timber harvesting and silvicultural practices. Individuals were selective in the location of their roosting areas, with both species selecting parts of the forest that contained higher densities of their preferred roost trees than was generally available in the forest. In contrast, in farmland at Naring, where there were small pockets of remnant vegetation with high densities of potential roost sites surrounded by cleared paddocks with few roosting opportunities, little selection was shown. This suggests that in Barmah forest the density of trees with potential roosts is lower than optimal, while in farmland roosting resources may be adequate in woodland remnants, but limiting at the landscape scale since more than 95% of the landscape now provides no roosting opportunities. Insectivorous bats appear to be less severely affected than some other faunal groups by habitat fragmentation and land-use change. A highly developed capacity for flight, the spatial scale at which they move and their ability to cross open areas means that they can regularly move among multiple landscape elements, rather than depend on single remnants for all their resources. In addition, bats forage and roost mainly at elevated levels in trees and so are less sensitive to degradation of wooded habitats at ground level. Although seemingly resilient to habitat fragmentation, insectivorous bats are fundamentally dependent on trees for roosting and foraging, and so are vulnerable to habitat loss and ongoing rural tree decline. Protection of the remaining large old trees and measures to ensure regeneration to provide ongoing replacement of hollow-bearing trees through time are critical to ensure the long-term conservation of bats in rural landscapes.

The use of molecular phylogenetic and morphological tools to identify cryptic and paraphyletic species : examples from the diminutive long-fingered bats (Chiroptera : Miniopteridae : Miniopterus) on Madagascar

Based on nearly complete (1125 bp) cytochrome-b sequence data and morphological characters, two new endemic species of Miniopterus are described from Madagascar that were previously identified as M. manavi. Using phylogenetic analysis, the basal nodes of major lineages in the Malagasy members of this genus are weakly supported, while, in most cases, the branches leading to each of the clades are well resolved. Miniopterus mahafaliensis, new species, occurs in the southwestern semidesert areas and M. brachytragos, new species, has a broad distribution across the northern half of the island, ranging across several different biomes. Phylogenetic inference indicates that these two new taxa are not closely related to M. manavi sensu stricto, with average genetic distances of 9.2% and 5.7% from this taxon, respectively. On the basis of this and previous revisions, the former M. manavi complex is now recognized to represent at least five taxa, which do not form a monophyletic group with respect to one another, and represent extraordinary examples of convergent evolution. Miniopterus brachytragos is closely related to the recently named M. aelleni, while M. mahafaliensis is not closely associated with any of these species. Molecular phylogenetic analysis was imperative to resolve the species limits of these taxa and morphology then provided the means to corroborate the recovered clades. There are localities on the island, specifically limestone karstic zones, where four species of the former M. manavi sensu lato complex occur in strict sympatry. These species often use the same day-roost caves and have similar external and craniodental measurements. This raises intriguing questions as to how these animals divide their worlds with regard to dietary regimes and foraging strategies, as well as their speciation history.

Morphological, bioacoustical, and genetic variation in Miniopterus bats from eastern Madagascar, with the description of a new species

Recent molecular genetic work, combined with morphological comparisons, of Malagasy members of the bat genus Miniopterus (Family Miniopteridae), has revealed several cryptic species. Based on new specimens and associated tissues, we examine patterns of variation in the recently described species M. petersoni, the holotype of which comes from extreme southeastern Madagascar, and for which specimens from more northerly portions of eastern Madagascar were noted to show some morphological divergence from typical M. petersoni. On the basis of morphological and genetic (cytochrome b) characters we described a new species, M. egeri sp. nov. This taxon also shows bioacoustical differences from M. petersoni. Miniopterus egeri is widely distributed in the eastern portion of Madagascar across an elevational range from near sea level to 550 m. The specific status of moderately small Miniopterus from Montagne d'Ambre in the far north remains to be determined.

Activity patterns of insectivorous bats and birds in northern Scandinavia (69° N), during continuous midsummer daylight

Previous studies suggest that many species of insectivorous bats are nocturnal, despite the relatively low availability of their insect prey at night, because of the risk of predation by diurnal predatory birds. We hypothesised that if this was the case bats living above the arctic circle would alter their feeding behaviour during midsummer because there would no longer be any benefit to restricting their activity to the period when their prey are least abundant. Alternatively, if bats were more influenced by competition from aerial insectivorous birds they would continue to feed at ‘night’ to avoid such competition. In northern Norway (69° N), during continuous midsummer daylight, insectivorous sand martins (Riparia riparia) concentrated their aerial feeding activity when aerial insects were most abundant. The birds stopped feeding between 23:00 and 07:00 when aerial insects were least abundant. In contrast, northern bats (Eptesicus nilssonii), fed mostly between 22:00 and 02:00, coinciding with the lowest aerial insect availability, and with the period when light levels were lowest (ca 1000 lux). Bat activity patterns were closest to those predicted by the avian competition hypothesis. The low densities of both sand martins and Northern bats in the study area, however, were less consistent with this hypothesis. Possibly populations of both species were higher historically and the observed patterns reflected historical competition. Bat activity was most closely correlated to ambient light levels. This raised two alternative explanations that we could not eliminate. Perhaps there was differential predation risk, between the brightest and darkest parts of the day, because the visual capacities of falcons are strongly dependent on luminance. Alternatively the bats may have been entrained to emerge at given light levels by their behaviour at other times of year.

Insights into the evolution of a cryptic radiation of bats: dispersal and ecological radiation of Malagasy Miniopterus (Chiroptera: Miniopteridae)

The past decade has seen a proliferation of new species of Miniopterus bats (family Miniopteridae) recognized from Madagascar and the neighboring Comoros archipelago. The interspecific relationships of these taxa, their colonization history, and the evolution of this presumed adaptive radiation have not been sufficiently explored. Using the mitochondrial cytochrome-b gene, we present a phylogeny of the Malagasy members of this widespread Old World genus, based on 218 sequences, of which 82 are new and 136 derived from previous studies. Phylogenetic analyses recovered 18 clades, which divide into five primary lineages: (1) M. griveaudi; (2) M. mahafaliensis, M. sororculus and X3; (3) M. majori, M. gleni and M. griffithsi; (4) M. brachytragos; M. aelleniA, and M. aelleniB; and (5) M. manavi and M. petersoni recovered as sister species, which were in turn linked to a group comprising M. egeri and five genetically distinct populations referred to herein as P3, P4, P5, P6 and P7. Beast analysis indicated that the initial divergence within the Malagasy Miniopterus radiation took place 4.5 Myr; most species diverged between 4 and 2.5 Myr, and a secondary period was between 1.25 and 1 Myr. DNA K2P-distances between recognized taxa ranged from 12.9% to 2.5% and intraspecific variation was less than 1.8%. Of the 18 identified clades, Latin binomials are only associated with 11, which indicates much greater differentiation than currently recognized for Malagasy Miniopterus. These data are placed in a context of the dispersal history of this genus on the island and patterns of ecological diversity.

A molecular and morphological investigation of species boundaries and phylogenetic relationships in Australian free-tailed bats Mormopterus (Chiroptera:Molossidae)

The taxonomic uncertainty surrounding several prominent genera of Australian microbat has been a long-standing impediment to research and conservation efforts on these groups. The free-tail bat genus Mormopterus is perhaps the most significant example, with a long history of acknowledged species-level confusion. This study uses a combined molecular and morphological approach to conduct a comprehensive assessment of species and subgeneric boundaries, between-species phylogenetic affinities and within-species phylogeographic structure in Australian members of Mormopterus. Phylogenetic analyses based on 759 base pairs of the NADH Dehydrogenase subunit 2 mitochondrial gene were concordant with species boundaries delineated using an expanded allozyme dataset and by phallic morphology, and also revealed strong phylogeographic structure within two species. The levels of divergence evident in the molecular and morphological analyses led us to recognise three subgenera within Australia: Micronomus, Setirostris subgen. nov. and Ozimops subgen. nov. Within Ozimops we recognise seven Australian species, three of which are new, and none are conspecific with Indo-Papuan species. The family Molossidae now comprises eleven species across three subgenera in Australia, making it the continent's second most speciose family of bats. © CSIRO 2014.