Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats

Cryptic species are similar in morphology, and make interesting subjects for relating morphological differentiation to ecological resource partitioning. Can species that are morphologically almost identical occupy different ecological niches, and hence potentially need distinct conservation planning? The discovery that the most widespread bat in Europe - the pipistrelle - comprised two cryptic species (Pipistrellus pipistrellus and Pipistrellus pygmaeus) that emit echolocation calls at different frequencies provides a remarkable model system for investigating links between morphology, echolocation call design and resource partitioning. We investigated resource partitioning between the two cryptic species of sympatric pipistrelle bats by radio tracking breeding females. Habitat selection was investigated by using compositional analysis. P. pygmaeus selected riparian habitats over all other habitat types in its core foraging areas, whereas P. pipistrellus, although preferring deciduous woodland overall, was more of a generalist, spreading its foraging time in a wider range of habitats. Although morphologically very similar, the cryptic species show quite different patterns of habitat use. Our findings suggest that large-scale differences in habitat preferences can occur between sympatric bat species that are virtually identical in flight morphology; hence morphological differences may be a weak indication of ecological differences between taxa. Conservation planning needs to take account of these differences to meet policy and legal obligations associated with these protected cryptic species.     

Improving the biodiversity benefits of hedgerows: How physical characteristics and the proximity of foraging habitat affect the use of linear features by bats

Within agricultural landscapes, linear features such as hedgerows and tree-lines provide valuable habitat for many species. We use data from 315 transects, completed as part of a national acoustic survey of bat distribution, to examine the incidence of four bat species adjacent to linear features in rural areas. The use of linear features was assessed in relation to hedgerow width, tree density, the presence of water and woodland proximity. To examine the effect of tree density, linear features were classified as either hedgerows without trees, hedgerows with sparse trees (comprising <50% tree canopy) or tree-lines (>50% tree canopy). The use of linear features by Pipistrellus pipstrellus was not affected by tree density; linear features of all types were associated with a similar increase in P. pipistrellus incidence. The use of linear features by Pipistrellus pygmaeus was dependent on both tree density and the proximity of woodland; only linear features containing trees provided an increase in P. pygmaeus incidence regardless of woodland proximity. P. pipistrellus and P. pygmaeus incidence was not affected by hedgerow width or the presence of water. Incidence of Nyctalus noctula and Eptesicus serotinus was unaffected by the density of linear features of any type. Many agri-environment schemes offer financial incentives for the creation and management of hedgerows. Optimising the biodiversity gain provided by linear features will maximise the effectiveness of these schemes. Agri-environment measures that encourage the provision and retention of hedgerow trees will benefit bats in agricultural landscapes.     

Habitat associations of bats in Northern Ireland: implications for conservation

Agricultural intensification in Northern Ireland has brought about large-scale changes to the landscape with a detrimental effect on biodiversity. Between 1996 and 1998, we surveyed a stratified random sample of 1 km squares for bats using a spot-sample technique and time expansion bat detector to establish linear and area habitat associations. Bats strongly selected water bodies with bankside vegetation, treelines, and deciduous and mixed woodland edge, avoiding open areas such as upland/unimproved grassland and improved grassland. Of three sympatric pipistrelle species (Pipistrellus pipistrellus, P. pygmaeus and P. nathusii), two were shown to forage in different habitats; P. pipistrellus being more of a ‘generalist’, foraging in a wider variety of habitats than P. pygmaeus, a ‘specialist’ which foraged in a smaller range of habitats. Nyctalus leisleri selected parkland/amenity grassland, deciduous woodland edge and rivers/canals and avoided improved grassland, hedgerows, whilst Myotis spp. selected deciduous woodland centre, lake/reservoir margins and rivers/canals. Reduction in area and quality of inland water, deciduous woodlands and field boundaries in Northern Ireland may impact on bat populations. Habitat management should focus on improving those habitats which are selected by bats, including the maintenance and enhancement of connecting linear habitats.     

Effects of landscape-scale broadleaved woodland configuration and extent on roost location for six bat species across the UK

Although forest fragmentation can greatly affect biodiversity, responses to landscape-scale measures of woodland configuration in Europe have been examined for only a limited range of taxa. Almost all European bat species utilise woodland, however little is known about how they are affected by the spatial arrangement of woodland patches. Here we quantify landscape structure surrounding 1129 roosts of six bat species and a corresponding number of control locations across the UK, to examine associations between roost location and landscape composition, woodland proximity and the size of the nearest broadleaved woodland patch. Analyses are performed at two spatial scales: within 1 km of the roost and within a radius equivalent to the colony home-range (3–7 km). For four species, models at the 1 km scale were better able to predict roost occurrence than those at the home-range scale, although this difference was only significant for Pipistrellus pipistrellus. For all species roost location was positively associated with either the extent or proximity of broadleaved woodland, with the greatest effect of increasing woodland extent seen between 0% and 20% woodland cover. P. pipistrellus, Pipistrellus pygmaeus, Rhinolophus hipposideros, Eptesicus serotinus and Myotis nattereri all selected roosts closer to broadleaved woodland than expected by chance, with 90% of roosts located within 440 m of broadleaved woodland. Roost location was not affected by the size of the nearest broadleaved patch (patches ranged from 0.06–2798 ha ± 126 SD). These findings suggest that the bat species assessed here will benefit from the creation of an extensive network of woodland patches, including small patches, in landscapes with little existing woodland cover.     

Scattered trees in rural landscapes: foraging habitat for insectivorous bats in south-eastern Australia

Scattered trees and small patches of vegetation among farmland are typical of rural landscapes throughout the world, often comprising a significant proportion of remaining habitats for native fauna. Insectivorous bats can use such isolated resources owing to the high mobility of most species, but little is known of the relationship between bats and tree density, or of the impact of incremental loss of trees in the landscape. Bats were surveyed at 30 sites in south-eastern Australia, in five habitat categories representing a range of tree densities from remnant woodland blocks (>35 trees/ha) to sparsely scattered trees (<1 tree/ha), and open paddocks devoid of trees. Sampling was undertaken by using harp traps and ultrasonic bat detectors. The abundance of potential arthropod prey was assessed by using light traps. Eleven species of insectivorous bats were recorded and bats were widespread in all habitat categories; all species were recorded around scattered trees. Overall activity, as revealed by detectors, did not differ significantly between the four treed categories, but in open paddocks there was a lower level of activity and a different community composition. However, a regression model revealed a significant quadratic relationship between activity of bats and tree density, with highest activity at 20-30 trees/ha. All species were recorded in open paddocks, but for eight of the ten species this represented <7% of their total activity recorded across all habitat categories. For six species, significant positive correlations were found between activity levels and the abundance of potential arthropod prey. In contrast to bat detectors, trapping results showed a significant difference in overall abundance of bats between wooded habitats, with decreased abundance as tree density declined. This study highlights the value of scattered trees as foraging habitat for bats, and emphasizes that, in rural land mosaics, such small and isolated habitat components have value for the conservation of biodiversity, and require greater recognition and protection.     

Influence of wetland networks on bat activity in mixed-use landscapes

Parks and other protected lands can provide important source habitat and act as valuable dispersal corridors in urbanizing environments. However, most wetlands within protected areas are managed in isolation without consideration of the broader landscape connections. We studied the importance of wetland habitat connectivity and landscape context to bat activity in five National Parks along a gradient of increasing urbanization within the Mid-Atlantic United States. Ninety-six Anabat stations were set up throughout the parks, from which we derived the characteristic spatial scales at which bat activity was associated with wetlands. This information was used in a graph theoretic framework to construct network models of potential landscape connectivity for those species that had positive associations with wetland land cover. We found that the importance of wetlands as a predictor of bat activity varied on a species-by-species basis and increased when network measures were used that accounted for connected area in a broad spatial context. The results demonstrate that both area and connectivity of wetland foraging habitat may act as orthogonal variables to availability of roosting habitat in explaining the distribution of highly mobile species. We use the results to illustrate the value of network analysis to guide the coordinated management of two of the parks’ most valued natural resources - wetlands and bats.     

Influence of prey variables, food supply, and river restoration on the foraging activity of Daubenton’s bat (Myotis daubentonii) in the Shibetsu River, a large lowland river in Japan

To conserve the foraging habitat of Daubenton’s bat (Myotis daubentonii) in a large lowland river, we investigated the influence on this bat of prey variables (number or biomass) and insect origin (aquatic or terrestrial). We tested the hypothesis that river restoration (re-meandering) conducted in the Shibetsu River, northern Japan, enhances foraging habitat quality by increasing the abundance of aquatic insects. From June to September 2004, flying insects were collected using Malaise traps in restored and channelised reaches in the Shibetsu River. Bat activity was recorded by bat detectors placed near the Malaise traps in each of the two reaches. Foraging activity of Daubenton’s bat was more strongly related to the number of insects than to biomass, and to adult aquatic insects than to terrestrial insects. The high dependence of Daubenton’s bat on aquatic prey was attributed to the fact that aquatic insect numbers were always higher than those of terrestrial insects. Contrary to the hypothesis, Daubenton’s bat was more active in the channelised reach than the restored reach in all months except June, and it synchronized its foraging activity with the seasonal distribution of adult aquatic insects. However, the study was undertaken just two years after restoration and the riparian vegetation had not yet established itself. Our results demonstrate the importance of aquatic insect abundance for Daubenton’s bat throughout the seasons in large lowland rivers. A further decrease in aquatic insects, associated with progressive anthropogenic alteration of river environments, undoubtedly exerts a harmful influence on the conservation of this species.     

Using multi-scale modelling to predict habitat suitability for species of conservation concern: The grey long-eared bat as a case study

Although spatial scale is important for understanding ecological processes and guiding conservation planning, studies combining a range of scales are rare. Habitat suitability modelling has been used traditionally to study broad-scale patterns of species distribution but can also be applied to address conservation needs at finer scales. We studied the ability of presence-only species distribution modelling to predict patterns of habitat selection at broad and fine spatial scales for one of the rarest mammals in the UK, the grey long-eared bat (Plecotus austriacus). Models were constructed with Maxent using broad-scale distribution data from across the UK (excluding Northern Ireland) and fine-scale radio-tracking data from bats at one colony. Fine-scale model predictions were evaluated with radio-tracking locations from bats from a distant colony, and compared with results of traditional radio-tracking data analysis methods (compositional analysis of habitat selection). Broad-scale models indicated that winter temperature, summer precipitation and land cover were the most important variables limiting the distribution of the grey long-eared bat in the UK. Fine-scale models predicted that proximity to unimproved grasslands and distance to suburban areas determine foraging habitat suitability around maternity colonies, while compositional analysis also identified unimproved grasslands as the most preferred foraging habitat type. This strong association with unimproved lowland grasslands highlights the potential importance of changes in agricultural practices in the past century for wildlife conservation. Hence, multi-scale models offer an important tool for identifying conservation requirements at the fine landscape level that can guide national-level conservation management practices.     

Species-specific barrier effects of a motorway on the habitat use of two threatened forest-living bat species

It is generally recognized that roads can adversely affect local animal populations but little is known how roads affect bats. In particular, no study compared the response of bats that differ in foraging ecology to motorways that cut through the breeding habitat. As bats are key species in conservation, such data are urgently needed for designing management plans. Using radio-telemetry, mist netting, and mark-recapture data we investigated the effects of a motorway with heavy traffic on the habitat use of two threatened forest-living bats. We compared barbastelle bats (Barbastella barbastellus), which forage in open space, to Bechstein’s bats (Myotis bechsteinii), which glean prey from the vegetation. Five of six radio-tracked barbastelle bats crossed the motorway during foraging and roost switching, flying through underpasses and directly over the motorway. In contrast, only three of 34 radio-tracked Bechstein’s bats crossed the motorway during foraging, all three using an underpass. Bechstein’s bats, unlike barbastelle bats, never crossed the motorway during roost switching. Moreover, only in Bechstein’s bats individuals foraging close to the motorway had smaller foraging areas than individuals foraging further away, whereas other forest edges had no such effect. Our data show that motorways can restrict habitat accessibility for bats but the effect seems to depend on the species’ foraging ecology and wing morphology. We suggest that motorways have stronger barrier effects on bats that forage close to surfaces than on bats that forage in open space, and discuss the implications of our findings for bat conservation during road construction.     

Influence of temperature in roost selection by Pipistrellus pygmaeus (Chiroptera): relevance for the design of bat boxes

The soprano pipistrelle (Pipistrellus pygmaeus) is a house-dwelling bat, whose maternity colonies are often affected by exclusion from buildings in southern Europe. Bat boxes with a suitable thermal behaviour can provide alternative roosts. However, this is particularly difficult to achieve in hot climates, where boxes may overheat. We studied roost temperatures and roost thermal preferences of this bat in attics and roofs in a Mediterranean region. Roosts reached high temperatures, experienced great thermal fluctuations and had wide spatial thermal ranges. Bats preferred the warmest locations within roosts, indicating that they are a heat tolerant species. However, they avoided temperatures of 40 °C and above, suggesting that this is the upper limit of the species thermally neutral zone. The study of experimental sets of white, grey and black boxes demonstrated that the latter were the ones that most often reached the temperatures observed in roosts in buildings. They were also the ones occupied by larger numbers of bats. These results suggest that, even in hot Mediterranean climates, black boxes are the best option as alternative roosts for evicted colonies. However, on particularly hot days, bats left them, suggesting that black boxes could be improved by creating a wider thermal range.     

The value of bat-boxes in the conservation of Pipistrellus pygmaeus in wetland rice paddies

Wetlands with rice paddies are key habitats in the conservation of biodiversity in the Mediterranean Region and are potentially suitable habitats for foraging bats, since they provide food (insects) and drinking places; nevertheless, many wetlands lack natural roosting sites. A bat-box program designed to ascertain bat-box preferences was initiated in 1999 in the Ebro Delta (NE Spain), one of the most important wetlands in Europe. A total of 69 bat-boxes of two types (single and double compartment) were placed on three supports (trees, houses, and posts) facing east or west. Pipistrellus pygmaeus occupancy rates and the number of individuals per box were monitored on 16 occasions from July 2000 to February 2004. Bat-box preferences were only detected during the breeding season. Bat abundance was higher in east-facing boxes, in double-compartment boxes, and in boxes placed on posts and houses. Boxes on natural supports (trees) were avoided. Bat-box occupancy rates were higher during the breeding season (95.6%, spring-summer) due to the formation of maternity colonies. The number of individuals in bat-boxes during the breeding season increased as the study period progressed (from summer 2000 to summer 2003), suggesting a high degree of acceptance by maternity colonies of these alternative locations. Occupancy rates observed were the highest ever reported in bat-box scientific literature. This study highlights the role of bat-box programs as useful alternative management tools for the conservation of bat populations in highly productive wetland habitats where few natural roost sites are available.     

Habitat management and patterns of predation of Northern Lapwings on wet grasslands: The influence of linear habitat structures at different spatial scales

In managed landscapes, habitat structure is frequently manipulated through the creation of features such as tracks, hedges, and waterways. If predator and prey activity are concentrated around these features, levels of predation may be elevated in these landscapes. This issue is of particular importance when habitat structures are used to attract species of conservation concern. For example, the installation of linear waterways in wet grasslands is a common form of habitat management to benefit breeding waders and wader nests and foraging chicks tend to be aggregated around wet features. If predator activity is also focused around these features, and if their linearity increases the probability of prey being located, then the conservation benefits of this management technique may be eliminated. We explore predator movement in relation to the structure and complexity of linear wet features within a lowland wet grassland landscape. We examine patterns of nest and chick predation in lapwing (Vanellus vanellus) at the whole-site, between-field and within-field scales. Mammalian predators were responsible for the majority of nest predation. However, we found no evidence that mammalian predators used linear wet features disproportionately within the landscape, or that wet feature distribution influenced the probability of nest or chick predation. At the whole-site scale, nest predation rates were significantly higher in areas with greater predator presence and lowest where the number of breeding neighbours was high. Thus, predation levels were influenced by large-scale patterns of predator presence and lapwing density but not by the use of linear wet features as a habitat management tool. Managing predator impacts is therefore likely to require empirical assessments of local predator distribution and abundance in order to target measures effectively.     

Small mammals in agricultural landscapes: Opposing responses to farming practices and landscape complexity

Organic farming often counteracts the decline of various taxa owing to agricultural intensification, but little is known about the relative importance of local management and landscape context for small mammals. We examined the abundance, species richness and diversity of small mammal communities in 22 organically and conventionally managed winter wheat fields pairwise located along a gradient of landscape structural complexity (41–94% arable land). Complex landscapes significantly increased small mammal abundance and (with marginal significance) species richness and diversity, but only in conventional fields, whereas organic farming increased small mammals in simple landscapes. These results indicate the importance of landscape complexity for small mammal populations in an intensified agriculture. Analyses at multiple spatial scales (100 m, 250 m, 500 m radii around focal fields), showed opposing responses of the three most abundant species to landscape complexity. Apodemus agrarius PALLAS abundance increased with increasing landscape complexity at a spatial scale of 100 m, whereas Microtus arvalis PALLAS and Sorex araneus L. abundances decreased with increasing landscape complexity at spatial scales of 100 m and 500 m, respectively, suggesting species-specific ecological needs as well as functional spatial scales for conservation management. In conclusion, agri-environmental measures for small mammals such as organic farming are most effective in simple landscapes, while complex landscapes presumably function as source habitats and can compensate for local agricultural intensification in conventional fields.     

Bat activity affected by sewage effluent in Irish rivers

Bat activity and benthic macroinvertebrates were sampled at nine paired sites, upstream and downstream from sewage effluent discharges into Irish rivers. Bat activity was measured using broadband acoustic detectors and macroinvertebrates by three 30-s standard benthic kick samples per site. Biological indices of water quality were significantly lower downstream from sewage outfalls, relative to upstream. The soprano pipistrelle (Pipistrellus pygmaeus) was significantly more active (as measured by bat passes per unit time) at downstream sites, while Daubenton’s bat (Myotis daubentonii) was less active. These results contrast with those of a similar study in England, where P. pygmaeus were less active, and Myotis spp. were more active downstream from sewage outfalls. We suggest that P. pygmaeus were more active downstream in our study because of a preference for preying on small orthocladiinid Chironomidae (non-biting midges), which were significantly more abundant downstream. M. daubentonii may prefer Trichoptera (caddis fly), which were significantly more abundant upstream. Organic pollution may then affect bats, but its effect appears to be more complex than previously implied. Implications of changing nutrient levels in freshwaters for populations of M. daubentonii and P. pygmaeus may be different from what is currently suggested in the literature.     

Scale-independent significance of river and riparian zones on three sympatric Myotis species in an agricultural landscape

Conserving biodiversity in agricultural landscapes is an urgent issue. The effective conservation of biodiversity requires plans based on species’ habitat preferences at multiple spatial scales. We examined how the foraging habitat selection of bats varied with grain size (50, 150, 250, and 350 m) and how habitat selection in the home range differed from that in the foraging habitat in an agricultural landscape. Focusing on three sympatric Myotis species (Myotis petax, Myotis gracilis, and Myotis frater), we radio-tracked 10 individuals of each species for 121 nights in Hokkaido, northern Japan. Rivers and broadleaved riparian forests were commonly preferred at multiple scales, although the preferred land-cover type was dependent on both extent and grain size for most species. The best grain sizes for predicting the foraging-habitat use of M. petax and M. gracilis were 50 and 150 m. By contrast, M. frater showed no tendency across the grain sizes. Our results indicate that it is necessary to consider both extent and grain size to understand the habitat selection of bats. Our findings also suggest that focusing primarily on preferred land-cover types at multiple scales is effective for conservation planning, given the limited resources in terms of time, manpower, and finances. Although arable did not negatively affect the selection of foraging habitats and home ranges in these bat species, preventing the loss of rivers and forests should be prioritized over preventing arable land expansion.     

The effects of illuminating the roost entrance on the emergence behaviour of Pipistrellus pygmaeus

In an attempt to increase the accuracy of roost emergence counts for a monitoring programme, the exits of two Pipistrellus pygmaeus roosts were illuminated with light of different colours and intensities. Light intensity affected bat emergence more than light colour. At one roost there was no significant difference in the bat emergence pattern between when the roost exit received no illumination and when it was illuminated with red light. The use of the latter is proposed to increase the accuracy of bat roost emergence counts.     

Effects of tropical forest fragmentation on aerial insectivorous bats in a land-bridge island system

Habitat fragmentation causes drastic changes in the biota and it is crucial to understand these modifications to mitigate its consequences. While studies on Neotropical bats have mainly targeted phyllostomid bats, impacts of fragmentation on the equally important aerial insectivores remain largely unexplored. We studied species richness, composition, count abundance and feeding activity of aerial insectivorous bats in a system of land-bridge islands in Panama with acoustic sampling. We predicted negative effects of fragmentation on forest species while bats foraging in open space should remain essentially unaffected. Rarefaction analyses indicated higher species richness for islands than mainland sites. For forest species, multivariate analyses suggested compositional differences between sites due to effects of isolation, area and vegetation structure. Contrary to our expectations, count abundance of forest species was similar across site categories. Feeding activity, however, was curtailed on far islands compared to near islands. As expected, bats hunting in open space did not reveal negative responses to fragmentation. Interestingly, they even displayed higher abundance counts on far and small islands. On the species level, two forest bats responded negatively to size reduction or site isolation, respectively, while a forest bat and a bat hunting in open space were more abundant on islands, irrespectively of island isolation or size. Our findings suggest that small forest remnants are of considerable conservation value as many aerial insectivores intensively use them. Hence high conservation priority should be given to retain or re-establish a high degree of forest integrity and low levels of isolation.     

Conservation value of forest fragments to Palaeotropical bats

Forested landscapes in Southeast Asia are becoming increasingly fragmented, making this region a conservation and research priority. Despite its importance, few empirical studies of effects of fragmentation on biodiversity have been undertaken in the region, limiting our ability to inform land-use regimes at a time of increased pressure on forests. We estimated the biodiversity value of forest fragments in peninsular Malaysia by studying fragmentation impacts on insectivorous bat species that vary in dependence of forest. We sampled bats at seven continuous forest sites and 27 forest fragments, and tested the influence of fragment isolation and area on the abundance, species richness, diversity, composition and nestedness of assemblages, and the abundance of the ten most common species. Overall, isolation was a poor predictor of these variables. Conversely, forest area was positively related with abundance and species richness of cavity/foliage-roosting bats, but not for that of cave-roosting or edge/open space foraging species. The smallest of fragments (<150 ha) were more variable in species composition than larger fragments or continuous forest, and larger fragments retained substantial bat diversity, comparable to continuous forest. Some fragments exhibited higher bat abundance and species richness than continuous forest, though declines might occur in the future because of time lags in the manifestation of fragmentation effects. Our findings suggest that fragments >300 ha contribute substantially to landscape-level bat diversity, and that small fragments also have some value. However, large tracts are needed to support rare, forest specialist species and should be the conservation priority in landscape-level planning. Species that roost in tree cavities or foliage may be more vulnerable to habitat fragmentation than those that roost in caves.