Do predators influence the behaviour of bats?

Many aspects of animal behaviour are affected by real‐time changes in the risk of predation. This conclusion holds for virtually all taxa and ecological systems studied, but does it hold for bats? Bats are poorly represented in the literature on anti‐predator behaviour, which may reflect a lack of nocturnal predators specialized on bats. If bats actually experience a world with minimal anti‐predator concerns, then they will provide a unique contrast within the realm of vertebrate ecology. Alternatively, such predator‐driven behaviour in bats may not yet be fully understood, given the difficulties in working with these highly mobile and nocturnal animals. We provide a wide‐ranging exploration of these issues in bat behaviour. We first cover the basic predator‐prey information available on bats, both on potential predators and the ways in which bats might perceive predators and respond to attacks. We then cover work relevant to key aspects of bat behaviour, such as choice of daytime roosts, the nature of sleep and torpor, evening roost departures, moonlight avoidance, landscape‐related movement patterns, and habitat selection. Overall, the evidence in favour of a strong influence of predators on bat behaviour is equivocal, with the picture clouded by contradictory results and a lack of information on potential predators and the perception of risk by bats. It seems clear that day‐active bats run a considerable risk of being killed by diurnal raptors, which are able to capture bats with relative ease. Thus, bats taking advantage of a pulse of insects just prior to sunset are likely taking risks to gain much‐needed energy. Further, the choice of daytime roosts by bats is probably strongly influenced by roost safety. Few studies, however, have directly addressed either of these topics. As a group, insectivorous temperate‐zone bats show no clear tendency to avoid apparently risky situations, such as activity on moonlit nights. However, some observations are consistent with the idea that predation risk affects choice of movement paths and feeding areas by temperate‐zone bats, as well as the timing of roost departures. The behaviour of tropical bats, on the other hand, seems more generally influenced by predators; this is especially true for tropical nectarivores and frugivores, but also for insectivorous bats. Presumably there are more serious predators on bats in the tropics (e.g. specialized raptors or carnivorous bats), but the identity of these predators is unclear. More information is needed to assess fully the influence of predators on bat behaviour. There is much need for work on the ways in which bats perceive predators via auditory, visual, and olfactory cues, and whether bats have some knowledge of the risks posed by different predators. Also needed is information on how predators attack bats and how bats react to attacking predators. Difficult to obtain, but of critical value, will be information on the nature of the predation risk experienced by bats while away from roosts and during the full darkness of night.     

Carnivorous bats?

Only large bats can take large prey but size alone does not identify 'carnivorous bats' (those including small terrestrial vertebrates in their diets). Morphological data, including body mass, aspect ratio and relative wing loading, along with information about orientation and foraging strategies can be used to characterize a suite of features which identifies carnivorous bats. We use the available data to make predictions about which large Microchiroptera will be found to be carnivorous. A combination of morphological features including body mass (^0.017 kg), low aspect ratio (<6.3), and low relative wing loading (<36) significantly identifies carnivorous species from among other animal-eating forms. Some carnivorous species use short, low intensity, high frequency, broadband echolocation cells but rely on prey generated cues to locate their targets. Other carnivorous species are facultative echolocators. The available data lead to the prediction that Phyllostomus hastatus and Hipposideros diadema are not regularly carnivorous, while Otonycteris hemprichi may be. Large species with echolocation calls adapted for flutter detection (rhinolophids and hipposiderids) or those with long narrowband calls and high aspect ratio wings with high relative wing loading (for example molossids, some emballonurids and some vespertilionids) chase airborne prey in the open; neither of these approaches involves prey other than arthropods.     

‘No cost of echolocation for flying bats’ revisited

Echolocation is energetically costly for resting bats, but previous experiments suggested echolocation to come at no costs for flying bats. Yet, previous studies did not investigate the relationship between echolocation, flight speed, aerial manoeuvres and metabolism. We re-evaluated the 'no-cost' hypothesis, by quantifying the echolocation pulse rate, the number of aerial manoeuvres (landings and U-turns), and the costs of transport in the 5-g insectivorous bat Rhogeessa io (Vespertilionidae). On average, bats (n = 15) travelled at 1.76 ± 0.36 m s?1 and performed 11.2 ± 6.1 U-turns and 2.8 ± 2.9 ground landings when flying in an octagonal flight cage. Bats made more U-turns with decreasing wing loading (body weight divided by wing area). At flight, bats emitted 19.7 ± 2.7 echolocation pulses s?1 (range 15.3-25.8 pulses s?1), and metabolic rate averaged 2.84 ± 0.95 ml CO? min?1, which was more than 16 times higher than at rest. Bats did not echolocate while not engaged in flight. Costs of transport were not related to the rate of echolocation pulse emission or the number of U-turns, but increased with increasing number of landings; probably as a consequence of slower travel speed when staying briefly on ground. Metabolic power of flight was lower than predicted for R. io under the assumption that energetic costs of echolocation call production is additive to the aerodynamic costs of flight. Results of our experiment are consistent with the notion that echolocation does not add large energetic costs to the aerodynamic power requirements of flight in bats.     

Does the survival of greater horseshoe bats and Geoffroy’s bats in Western Europe depend on traditional cultural landscapes?

Greater horseshoe bats (Rhinolophus ferrumequinum) and Geoffroy’s bats (Myotis emarginatus) are two sympatric species that have undergone a serious population decline in Central Europe. In both species, population decline is likely to have been caused by habitat deterioration and habitat loss resulting in a decrease of carrying capacity. We examined the spatial ecology, habitat use and key landscape features in vital populations in R. ferrumequinum and M. emarginatus in the northern part of their current European distribution in Luxembourg. In total, 3,559 fixes from 26 radiotracked individuals were calculated. The tracked individuals of both species showed commuting flights along hedgerows, streams and small-forested patches. Maximum flight distances, home range sizes and habitat diversity did not differ between species, but R. ferrumequinum had significantly larger foraging ranges than adult M. emarginatus. Contrary to other studies, both bat species preferred semi-open, but richly structured traditional farmland habitats such as orchards, pastures and parkland habitats instead of available large broad-leaved deciduous forests. M. emarginatus frequently preyed on abundant arthropod resources in cowsheds, sometimes even exclusively throughout the night. The landscape configuration around the buffered radio fixes of adult R. ferrumequinum and M. emarginatus differed significantly from that around analysed random buffers. Radio fixes were concentrated in a landscape characterised by higher habitat diversity than in the surrounding region. Our results support the concept of a ‘biocultural link’ between traditional land use and biodiversity, and we therefore strongly recommend the conservation of extensive traditional land use practices, which will help to preserve both endangered bat species along with the local biodiversity.     

Population structure of Daubenton’s bats is responding to microclimate of anthropogenic roosts

Roost microclimate plays an important role in the survival, growth and reproduction in microbats. Entering torpor is one of the main energy saving mechanisms commonly used by microbats. The use of torpor is affected by roost microclimate and seasonally differs between the two sexes in relation to their reproductive condition. Consequently, thermal properties of male and female roosts should differ. To test this hypothesis, we compared temperature parameters of two anthropogenic day roosts of Daubenton’s bats with a different structure of the population inhabiting them. In accordance with our predictions, the roost occupied by a male-dominated colony was colder and more fluctuant than the maternity roost with a female-dominated population. However, using of the two roosts changed during the season in response to changing energetic demands of the two sexes. While males were almost absent in the warmer maternity roost during pregnancy and lactation, they appeared in this roost during the post-lactation when mating starts. In contrast, females did not use the colder (male) roost until the time of weaning of juveniles, i.e., the time when their thermoregulatory needs change and they may benefit from using colder roost. Our study provides the evidence that the same roost may be used by individuals of different sex and reproductive state in different periods of the year. Generalizations about roost selection without knowledge of temporal variation in roost use and microclimatic conditions should be taken with caution. Anthropogenic roosts may be advantageous to Daubenton’s bats as these can provide a variety of suitable microclimates and/or more space for roosting than tree cavities.     

Mortality of bats at wind turbines links to nocturnal insect migration?

This note is based on a literature search and a recent review of bat mortality data from wind farms in Europe (published elsewhere). We suggest that mortality of bats at wind turbines may be linked to high-altitude feeding on migrating insects that accumulate at the turbine towers. Modern wind turbines seem to reach high enough into the airspace to interfere with the migratory movements of insects. The hypothesis is consistent with recent observations of bats at wind turbines. It is supported by the observation that mortality of bats at wind turbines is highly seasonal (August–September) and typically peaks during nights with weather conditions known to trigger large-scale migratory movements of insects (and songbirds). We also discuss other current hypotheses concerning the mortality of bats at wind turbines.     

Characteristics of echolocating bats’ auditory stereocilia length, compared with other mammals

The stereocilia of the Organ of Corti in 4 different echolocating bats, Myotis adversus, Murina leucogaster, Nyctalus plancyi (Nyctalus velutinus), and Rhinolophus ferrumequinum were observed by using scanning electron microscopy (SEM). Stereocilia lengths were estimated for comparison with those of non-echolocating mammals. The specialized lengths of outer hair cells (OHC) stereocilia in echolocating bats were shorter than those of non-echolocating mammals. The specialized lengths of inner hair cells (IHC) stereocilia were longer than those of outer hair cells stereocilia in the Organ of Corti of echolocating bats. These characteristics of the auditory stereocilia length of echolocating bats represent the fine architecture of the electromotility process, helping to adapt to high frequency sound and echolocation. These authors contributed equally to this work Supported by the National Natural Science Foundation of China (Grant No. 30430120) and Foundation of President of the Chinese Academy of Sciences     

Characteristics of echolocating bats’auditory stereocilia length, compared with other mammals

The stereocilia of the Organ of Corti in 4 different echolocating bats, Myotis adversus, Murina leuco-gaster, Nyctalus plancyi (Nyctalus velutinus), and Rhinolophus ferrumequinum were observed by using scanning electron microscopy (SEM). Stereocilia lengths were estimated for comparison with those of non-echolocating mammals. The specialized lengths of outer hair cells (OHC) stereocilia in echolocating bats were shorter than those of non-echolocating mammals. The specialized lengths of inner hair cells (IHC) stereocilia were longer than those of outer hair cells stereocilia in the Organ of Corti of echolocating bats. These characteristics of the auditory stereocilia length of echolocating bats represent the fine architecture of the electromotility process, helping to adapt to high frequency sound and echolocation.     

Characteristics of echolocating bats’ auditory stereocilia length,compared with other mammals

The stereocilia of the Organ of Corti in 4 different echolocating bats, Myotis adversus, Murina leucogaster, Nyctalus plancyi (Nyctalus velutinus), and Rhinolophus ferrumequinum were observed by using scanning electron microscopy (SEM). Stereocilia lengths were estimated for comparison with those of non-echolocating mammals. The specialized lengths of outer hair cells (OHC) stereocilia in echolocating bats were shorter than those of non-echolocating mammals. The specialized lengths of inner hair cells (IHC) stereocilia were longer than those of outer hair cells stereocilia in the Organ of Corti of echolocating bats. These characteristics of the auditory stereocilia length of echolocating bats represent the fine architecture of the electromotility process, helping to adapt to high frequency sound and echolocation.     

Sulphur-containing “perfumes” attract flower-visiting bats

 We tested the attractiveness of individual scent compounds of bat-pollinated flowers to their pollinators, small flower-visiting bats of the genus Glossophaga (Phyllostomidae). Twenty compounds belonging to four different chemical substance classes were tested, both in the laboratory and in the field. In the laboratory, the bats (Glossophaga soricina) approached odour sources spontaneously and without preceding experience. Without ever receiving any reward they preferred the scent of a sulphur-containing compound, dimethyl disulphide, to several other odour components emitted by bat-pollinated flowers, and to scentless controls. In the field, at La Selva station in the tropical lowland rain forest of Costa Rica, G. commissarisi were attracted by two sulphur-containing compounds, dimethyl disulphide and 2,4-dithiapentane, to visit artificial flowers filled with sugar water. Thus, in nectarivorous bats the sense of smell obviously plays an important role in searching for and localising food sources, and even single components of the scent bouquets of bat-pollinated flowers are attractive. The preference for sulphur-containing odours seems to be innate. Accepted: 9 November 1999     

Field metabolic rates of phytophagous bats: do pollination strategies of plants make life of nectar-feeders spin faster?

Recently, it was argued that extrinsic factors, such as high foraging costs, lead to elevated field metabolic rates (FMR). We tested this suggestion by comparing the FMR of nectar-feeding and fruit-eating bats. We hypothesized that the foraging effort per energy reward is higher for nectar-feeding mammals than for fruit-eating mammals, since energy rewards at flowering plants are smaller than those at fruiting plants. Using the doubly labelled water method, we measured the FMR of nectar-feeding Glossophaga commissarisi and fruit-eating Carollia brevicauda, which coexisted in the same rainforest habitat and shared the same daytime roosts. Mass-specific FMR of G. commissarisi exceeded that of C. brevicauda by a factor of almost two: 5.3±0.6 kJ g⁻¹ day⁻¹ for G. commissarisi and 2.8±0.4 kJ g⁻¹ day⁻¹ for C. brevicauda. Since nectar-feeding bats imbibe nectar droplets of only 193 J energy content during each flower visit, a G. commissarisi bat has to perform several 100 flower visits per night to meet its energy requirement. The fruit-eating C. brevicauda, on the other hand, needs to harvest only 3–12 Piper infructescenses per night, as the energy reward per Piper equals ca. 6–30 kJ. We argue that the flowering and fruiting plants exert different selective forces on the foraging behaviour and energetics of pollinators and the seed dispersers, respectively. A comparison between nectar-feeding and non-nectar-feeding species in various vertebrate taxa demonstrates that pollinators have elevated FMRs.     

Spatial and temporal analysis of α, β and γ diversities of bats in a fragmented landscape

We test a strategy for analyzing species richness in a landscape. This strategy is based on the joint analysis of (local), (turnover) and (landscape) diversities. We assessed the spatial and temporal relations among , and diversity of bats (Phyllostomidae and Mormoopidae) in a tropical landscape. In a spatial dimension, diversity depends on the diversity of the most species-rich community. The value of spatial diversity between habitats was very low. A high diversity was found in a cornfield, which may be attributed to the reduced extent of the field (compared with a more extensive field) that allows the arrival of individuals from nearby rich communities. In a temporal dimension, within habitat cumulative richness over sampling period may be considerably different from the average richness. These differences are attributed to temporal turnover during short time intervals. Therefore, cumulative richness may be viewed as the temporal equivalent of within-habitat diversity, which results of both average and temporal turnover. We discuss, which value must be taken as an estimate of habitat species richness, the average or the cumulative , and the implications that this decision can have in the evaluation of biodiversity.     

Audiovocal interactions during development? Vocalisation in deafened young horseshoe bats vs. audition in vocalisation-impaired bats

Summary Horseshoe bats (Rhinolophus rouxi) were deafened in their 3rd–5th postnatal week. Subsequently their vocalisations were monitored to evaluate the impact of audition on the development of echolocation pulses. Hearing impairment affected the echolocation pulses as follows: the frequency of the constant frequency (CF) component was altered by between + 4 kHz and – 14 kHz, and the dominance of the second harmonic of the pulses was neutralised by a relative increase in intensity of the first and third harmonics.A second experiment focused on possible influences of acoustical self-stimulation with echolocation pulses on the establishment of auditory fovea representation in the inferior colliculus (IC). Frequency control of echolocation pulses was disrupted by larynx denervation. Thereafter, the bats produced multiharmonic echolocation signals (4–11 harmonics) varying in frequency. IC tonotopy, however, as monitored by stereotaxic electrophysiology, showed the same developmental dynamics as seen in control specimens (Fig. 10).Both experiments indicate that throughout postnatal development echolocation pulses are under auditory feedback control, whereas maturation of the auditory fovea and shifts in its frequency tuning represent an innate process. The significance of this postnatal development might be the adjustment of the vocal motor system of each bat to the frequency of its personal auditory fovea.Abbreviations CF constant frequency - CF1, CF2, CF3 harmonics of pure tone components of the echolocation pulses - FM frequency modulation - IC inferior colliculus of the midbrain     

Changes in abundance of hibernating bats in central Slovakia (1992–2009)

An analysis of long-term changes in abundance of hibernating bats as revealed from the annual monitoring programme conducted in four mountain regions of the Western Carpathians (Muránska planina Mts, Revúcka vrchovina Mts, Slovensky kras Mts, Štiavnické vrchy Mts) during the period 1992–2009 is providing in the paper. Data from 52 hibernacula were analysed. Among 18 bat species recorded, an apparent population increase of three most abundant thermophilous and originally cave dwelling species of bats, Rhinolophus hipposideros, R. ferrumequinum, Myotis myotis, was observed. In other bat species (e.g., R. euryale, M. emarginatus, M. mystacinus, M. dasycneme, Barbastella barbastellus), population trends could not be detected and because of data scarcity, they should be evaluated from more extensive datasets obtained from a wide range of hibernacula or from a completely different type of evidence.     

Conserving energy at a cost to biodiversity? Impacts of LED lighting on bats

Artificial lighting is a key biodiversity threat and produces 1900 million tonnes of CO ₂ emissions globally, more than three times that produced by aviation. The need to meet climate change targets has led to a global increase in energy‐efficient light sources such as high‐brightness light‐emitting diodes (LEDs). Despite the energetic benefits of LEDs, their ecological impacts have not been tested. Using an experimental approach, we show that LED street lights caused a reduction in activity of slow‐flying bats ( Rhinolophus hipposideros and Myotis spp.). Both R. hipposideros and Myotis spp. activities were significantly reduced even during low light levels of 3.6 lux. There was no effect of LED lighting on the relatively fast‐flying Pipistrellus pipistrellus, Pipistrellus pygmaeus and Nyctalus/Eptesicus spp. We provide the first evidence of the effects of LED lights on bats. Despite having considerable energy‐saving benefits, LED lights can potentially fragment commuting routes for bats with associated negative conservation consequences. Our results add to the growing evidence of negative impacts of lighting on a wide range of taxa. We highlight the complexities involved in simultaneously meeting targets for reduction of greenhouse gas emissions and biodiversity loss. New lighting strategies should integrate climate change targets with the cultural, social and ecological impacts of emerging lighting technologies.     

Ultrasound detection in fish--a parallel to the sonar-mediated detection of bats by ultrasound-sensitive insects?

Most bats use ultrasonic sonar signals, or cries, to locate prey. Many of their insect prey species have evolved an ability to hear and respond to these signals, and studies clearly demonstrate the survival value associated with this ability. Like bats, toothed whales locate prey by emitting ultrasonic sonar signals, or clicks. As a parallel to the insect prey of bats, it would seem obvious to assume that some fish species likewise are capable of sensing the ultrasonic clicks of their odontocete predators. As judged from classical fish audiometry literature, this seems not to be the case, however, and although in recent years some fishes have been proven responsive to ultrasound, examination of ecological and acoustic differences reveals that conclusions on ultrasound-mediated insect escape behavior are not immediately applicable to fish. This has the consequence that future experiments on fish ultrasound detection should not be looking for observations directly parallel to those observed in the bat-insect interactions.     

The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern?

The peak echolocation frequency of insectivorous bats generally declines as body size increases. However, there are notable exceptions to this rule, with some species, such as Rhinolophus clivosus, having a higher than expected peak frequency for their body size. Such deviations from allometry may be associated with partitioning of foraging habitat (the foraging habitat hypothesis) or insect prey (the prey detection hypothesis). Alternatively, the deviations may be associated with the partitioning of sonar frequency bands to allow effective communication in a social context (the acoustic communication hypothesis). We tested the predictions of these hypotheses through comparisons at the family, clade and species level, using species of rhinolophids in general and R. clivosus, a species with a wide distribution, as a specific test case. We compared the wing parameters, echolocation frequency and ecology of R. clivosus to those of the sympatric R. capensis. Rhinolophus clivosus has a much higher echolocation frequency than predicted from its wing loading or body mass. Furthermore, contrary to the predictions of the foraging habitat hypothesis, we found no difference in foraging habitat between R. clivosus and R. capensis. The size range of insect prey taken by the two species also overlapped almost completely, contrary to the prey detection hypothesis. On the other hand, the variation of echolocation frequencies around the allometric relationship for rhinolophids was smaller than that for Myotis spp., supporting the prediction of the acoustic communication hypothesis. We thus propose that the relatively high peak frequency of R. clivosus is the result of partitioning of sonar frequency bands to minimize the ambiguity of echolocation calls during social interactions.     

The energy cost of flight: do small bats fly more cheaply than birds?

Flapping flight is one of the most expensive activities in terms of metabolic cost and this cost has previously been considered equal for the two extant vertebrate groups which evolved flapping flight. Owing to the difficulty of obtaining accurate measurements without disturbing flight performance, current estimates of flight cost within the group of small birds and bats differ by more than a factor of five for given body masses. To minimize the potential problem that flight behaviour may be affected by the measurements, we developed an indirect method of measuring flight energy expenditure based on time budget analysis in which small nectar-feeding bats (Glossophaginae) could continue their natural rhythm of flying and resting entirely undisturbed. Estimates of metabolic flight power based on 172 24-h time and energy budget measurements were obtained for nine individual bats from six species (mass 7–28 g). Metabolic flight power (P_F) of small bats was found to increase with body mass following the relation P_F = 50.2 M^0.771 (r² = 0.96, n = 13, P_F in W, M in kg). This is about 20–25% below the majority of current predictions of metabolic flight cost for small birds. Thus, either the flight cost of small birds is significantly lower than has previously been thought or, contrary to current opinion, small bats require less energy to fly than birds. Accepted: 29 September 1997