Greater Horseshoe Bat Research Articles

Autumn flight activity of the greater horseshoe bat at hibernacula

The activity patterns of vespertilionid bats at the entrances of hibernacula in temperate zones have been investigated on many occasions. However, little is known about nocturnal flight activity in autumn and its function in horseshoe bats so far. Here, we have recorded the autumn flight activity in and around the entrances of hibernacula of greater horseshoe bats,Rhinolophus ferrumequinumby behavioural observations, mistnetting, and acoustic surveys for two consecutive years. Greater horseshoe bats not only chased each other around cave entrances but also entered and left the entrance frequently. However, no mating events were directly observed in this study, normally a prominent part of swarming behaviour in vespertilionids. Therefore, it is difficult to deduce the function of the autumn flight activity of the greater horseshoe bats at hibernacula from the present data. Additionally, the recorded flight activity was positively correlated with ambient temperature and humidity. To our knowledge, our study provides the first detailed record of the pattern of autumn flight activity in horseshoe bats, and suggests that weather conditions may impact the bats’ nocturnal flight activity.

High duty cycle pulses suppress orientation flights of crambid moths

Bat-and-moth is a good model system for understanding predator–prey interactions resulting from interspecific coevolution. Night-flying insects have been under predation pressure from echolocating bats for 65Myr, pressuring vulnerable moths to evolve ultrasound detection and evasive maneuvers as counter tactics. Past studies of defensive behaviors against attacking bats have been biased toward noctuoid moth responses to short duration pulses of low-duty-cycle (LDC) bat calls. Depending on the region, however, moths have been exposed to predation pressure from high-duty-cycle (HDC) bats as well. Here, we reveal that long duration pulse of the sympatric HDC bat (e.g., greater horseshoe bat) is easily detected by the auditory nerve of Japanese crambid moths (yellow peach moth and Asian corn borer) and suppress both mate-finding flights of virgin males and host-finding flights of mated females. The hearing sensitivities for the duration of pulse stimuli significantly dropped non-linearly in both the two moth species as the pulse duration shortened. These hearing properties support the energy integrator model; however, the threshold reduction per doubling the duration has slightly larger than those of other moth species hitherto reported. And also, Asian corn borer showed a lower auditory sensitivity and a lower flight suppression to short duration pulse than yellow peach moth did. Therefore, flight disruption of moth might be more frequently achieved by the pulse structure of HDC calls. The combination of long pulses and inter-pulse intervals, which moths can readily continue detecting, will be useful for repelling moth pests.

Mandibular and cranial modularity in the greater horseshoe bat Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae)

We report the first evaluation of mandibular and cranial modularity in the greater horseshoe bat ( Rhinolophus ferrumequinum ). Although some authors found no modular pattern of these morphological structures in mammals, we discovered that traits integration in R. ferrumequinum is not uniform throughout the mandible and cranium, but structured into two distinct modules. Allometry does not affect mandibular and cranial modularity in R. ferrumequinum probably as a result of the low fraction of shape variation explained by size. Observed at the static level, mandible and cranium modularity in this species could be either functional or developmental or both, but we cannot rule out a genetic nature for underlying mandibular and cranial trait interactions. Evolutionary modularity among related taxa is influenced by genetic and functional modularity. Therefore, future studies on cranial integration and modularity at multiple levels of variation may shed more light on these important features of morphological variability in bats, including R. ferrumequinum . Download the complete issue.

Sexual signaling under predation: attractive moths take the greater risks

Individuals often have to balance the costs of risky behavior against the potential benefits they may gain from it. This trade-off is especially obvious in the interplay between natural and sexual selection because traits for mate attraction may attract predators as well. In the lesser wax moth Achroia grisella, ultrasonic sexual signaling comes with such a risk because calling for mates also attracts predatory bats. Attractive males should behave more cautiously than unattractive males under such circumstances, as they can expect more future mating opportunities and therefore have more to lose (the so-called asset protection principle). Contrary to these predictions, we found that pulse pair rate and peak amplitude, 2 song components attractive to females, correlated negatively with the duration of a silence response which is displayed when courtship song is experimentally overlayed with the search signal of a predator, the greater horseshoe bat. More attractive males thus recommence singing sooner than less attractive males. Although this is not in line with the asset protection principle, we discuss 3 different ways in which these distinct behavioral differences might be explained: 1) attractive males are in better condition and thus can more easily evade predators, 2) attractive signals are costly in terms of reduced life expectancy, and 3) risk-taking may in itself be a sexually selected trait and as such act as an honest signal of male quality.

A test of Rensch's rule in greater horseshoe bat (Rhinolophus ferrumequinum) with female-biased sexual size dimorphism.

Sexual size dimorphism (SSD) is widespread within the animal kingdom. Rensch’s rule describes a relationship between SSD and body size: SSD increases with body size when males are the larger sex, and decreases with body size when females are the larger sex. Rensch’s rule is well supported for taxa that exhibit male-biased SSD but patterns of allometry among taxa with female-biased size dimorphism are mixed, there is evidence both for and against the rule. Furthermore, most studies have investigated Rensch’s rule across a variety of taxa; but among-population studies supporting Rensch’s rule are lacking, especially in taxa that display only slight SSD. Here, we tested whether patterns of intraspecific variation in SSD in greater horseshoe bats conform to Rensch’s rule, and evaluated the contribution of latitude to Rensch’s rule. Our results showed SSD was consistently female-biased in greater horseshoe bats, although female body size was only slightly larger than male body size. The slope of major axis regression of log10 (male) on log10 (female) was significantly different from 1. Forearm length for both sexes of greater horseshoe bats was significantly negatively correlated with latitude, and males displayed a slightly but nonsignificant steeper latitudinal cline in body size than females. We suggest that variation in patterns of SSD among greater horseshoe bat populations is consistent with Rensch’s rule indicating that males were the more variable sex. Males did not have a steeper body size–latitude relationship than females suggesting that sex-specific latitudinal variation in body size may not be an important contributing factor to Rensch’s rule. Future research on greater horseshoe bats might best focus on more comprehensive mechanisms driving the pattern of female-biased SSD variation.

Where and at What Time? Multiple Roost use and Emergence Time in Greater Horseshoe Bats (Rhinolophus ferrumequinum)

One of the largest nursery colonies of Rhinolophus ferrumequinum in Italy occurs in the Natural Park of Migliarino San Rossore Massaciuccoli, Tuscany, with the species roosting in several buildings. We identified various roosts used by R. ferrumequinum within the park and investigated their microclimatic parameters (temperature, relative humidity and daily temperature excursion). We monitored roost use for one year and found it not only to be influenced by season and the microclimatic conditions of different roosts, but also by occasional stress conditions such as disturbance by predators. We also studied nightly emergence behavior, specifically we considered how this is influenced by climatic (temperature, relative humidity and evening light intensity) and demographic (presence of pups, subadults and colony size) parameters. The colony always performed a pre-emergence behavior and we found that its onset occurred earlier at higher temperatures, lower evening light intensity, in larger colonies and in the presence of pups. High temperature and low evening light intensity also resulted in a longer nightly emergence, which was also identified in larger colonies and when subadults were present. This study highlights the importance of the conservation of multiple roosts within the distribution range of R. ferrumequinum nurseries. Additionally, we demonstrated how certain climatic and demographic factors influence both pre-emergence and emergence behavior.

Different Auditory Feedback Control for Echolocation and Communication in Horseshoe Bats

Auditory feedback from the animal's own voice is essential during bat echolocation: to optimize signal detection, bats continuously adjust various call parameters in response to changing echo signals. Auditory feedback seems also necessary for controlling many bat communication calls, although it remains unclear how auditory feedback control differs in echolocation and communication. We tackled this question by analyzing echolocation and communication in greater horseshoe bats, whose echolocation pulses are dominated by a constant frequency component that matches the frequency range they hear best. To maintain echoes within this “auditory fovea”, horseshoe bats constantly adjust their echolocation call frequency depending on the frequency of the returning echo signal. This Doppler-shift compensation (DSC) behavior represents one of the most precise forms of sensory-motor feedback known. We examined the variability of echolocation pulses emitted at rest (resting frequencies, RFs) and one type of communication signal which resembles an echolocation pulse but is much shorter (short constant frequency communication calls, SCFs) and produced only during social interactions. We found that while RFs varied from day to day, corroborating earlier studies in other constant frequency bats, SCF-frequencies remained unchanged. In addition, RFs overlapped for some bats whereas SCF-frequencies were always distinctly different. This indicates that auditory feedback during echolocation changed with varying RFs but remained constant or may have been absent during emission of SCF calls for communication. This fundamentally different feedback mechanism for echolocation and communication may have enabled these bats to use SCF calls for individual recognition whereas they adjusted RF calls to accommodate the daily shifts of their auditory fovea.

The complete mitochondrial DNA genome of a greater horseshoe bat subspecies, Rhinolophus ferrumequinum quelpartis (Chiroptera: Rhinolophidae)

There are two subspecies of Rhinolophus ferrumequinum currently recognized in South Korea. The Korean greater horseshoe bat subspecies, Rhinolophus ferrumequinum quelpartis, is distributed only in Jeju Island. The complete mitochondrial genome of the island subspecies was determined and revealed 99.7% similarity to the mainland subspecies Rhinolophus ferrumequinum korai. If d-loop region is excluded, similarity of the two genomes was 99.9%.

Noseleaf Dynamics during Pulse Emission in Horseshoe Bats

Horseshoe bats emit their biosonar pulses nasally and diffract the outgoing ultrasonic waves by conspicuous structures that surrounded the nostrils. Here, we report quantitative experimental data on the motion of a prominent component of these structures, the anterior leaf, using synchronized laser Doppler vibrometry and acoustic recordings in the greater horseshoe bat (Rhinolophus ferrumequinum). The vibrometry data has demonstrated non-random motion patterns in the anterior leaf. In these patterns, the outer rim of the walls of the anterior leaf twitches forward and inwards to decrease the aperture of the noseleaf and increase the curvature of its surfaces. Noseleaf displacements were correlated with the emitted ultrasonic pulses. After their onset, the inward displacements increased monotonically towards their maximum value which was always reached within the duration of the biosonar pulse, typically towards its end. In other words, the anterior leaf’s surfaces were moving inwards during most of the pulse. Non-random motions were not present in all recorded pulse trains, but could apparently be switched on or off. Such switches happened between sequences of consecutive pulses but were never observed between individual pulses within a sequence. The amplitudes of the emitted biosonar pulse and accompanying noseleaf movement were not correlated in the analyzed data set. The measured velocities of the noseleaf surface were too small to induce Doppler shifts of a magnitude with a likely significance. However, the displacement amplitudes were significant in comparison with the overall size of the anterior leaf and the sound wavelengths. These results indicate the possibility that horseshoe bats use dynamic sensing principles on the emission side of their biosonar system. Given the already available evidence that such mechanisms exist for biosonar reception, it may be hypothesized that time-variant mechanisms play a pervasive role in the biosonar sensing of horseshoe bats.

The conservation genetics of three cave-dwelling bat species in southeastern Europe and Anatolia

Genetic data from populations are currently being used in order to assess the conservation status of various species. In this study, the conservation implications of the genetic structure of 3 cave-dwelling bat species in southeastern Europe and Anatolia are discussed. These species are the greater horseshoe bat (Rhinolophus ferrumequinum), the bent-winged bat (Miniopterus schreibersii), and the long-fingered bat (Myotis capaccinii). The conservation status of the species is evaluated using 3 conservation unit approaches, specifically evolutionarily significant unit and management unit definitions and population aggregation analysis. These approaches are implemented simultaneously for the first time for any species in Turkey, through an evaluation of mitochondrial and nuclear DNA data previously generated for these species. Based on these data, both regional and cave-specific conservation recommendations are made. The results suggest that for M. capaccinii, the area to be protected in order to maximize the conservation of genetic diversity is around the border of Turkey with Bulgaria and Greece. For the other 2 species, these areas are within Anatolia.

Seasonal habitat use by greater horseshoe bat Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae) in Changbai Mountain temperate forest, Northeast China

Abstract We performed acoustic surveys at 78 sites around one bat colony to examine seasonal patterns of habitat use by greater horseshoe bats. Insect abundance and temperature were determined in each season. Bat diets were assessed by analysing faecal composition. Greater horseshoe bats tended to forage in mixed broadleaved and mixed broadleaved and coniferous woodland and were rarely found foraging in coniferous woodland. Bat activity in mixed broadleaved woodland and woodland glades significantly decreased from June to September. There were significant seasonal differences in the frequency of utilization of different habitats. Distance from the day roost had significant effects on bat activity only in June and July. The diet of greater horseshoe bats was clearly dominated by Lepidoptera and Coleoptera, with some variations with seasons. The seasonal variation of habitat use by greater horseshoe bats probably depended on resource availability that fluctuates over space and time. These results have important implications for the conservation of this bat species. Cluttered broadleaved woodland and mixed broadleaved woodland constitute an important target for conservation. Instead of reforestation with the non-native pure coniferous woodland, planting and maintaining broadleaved forests or mixed forests should be encouraged.

Ear deformations in the biosonar system of horseshoe bats.

Many bat species exhibit conspicuous ear movements as part of their biosonar behaviors. The resulting transformations of the pinnae can contain rigid rotations as well as nonrigid deformations. Characteristic ear deformations are frequently observed in horseshoe bats (Rhinolophidae). In these animals, the pinna changes regularly between an upright and a bent configuration. In the bent configuration, the tip of the pinna tilts forward, down, and sideways, changing the curvature of large portions of the ear surface. Entire deformation cycles can be completed in as little as 200 ms. The time-variant geometry of the pinna deformations in the greater horseshoe bat (Rhinolophus ferrumequinum) was captured with a stereo pair of high-speed video cameras. Landmark points were marked on the pinna with dyes that were equally visible in the video frames as in x-ray micro-CT. The CT model was matched to the locations of the landmarks in the deforming ears inferred from stereo reprojection. Numerical predictions were obtained for the acoustic behavior of ear shapes at different phases during the deformation cycle. It was found that the pinna deformations seen in the animals can produce large changes in the directivity patterns. [Work supported by NSFC (Project No. 10774092) and CSC.]

First record of four species of bats from the nationale park of El Feidja (NW Tunisia) with a note on the non-flying mammals of the Khroumiria region

During a field study carried out in the Tunisian National Park of El Feidja (Khroumiria region, NW Tunisia) in May 2000, we captured four species of bats never previously recorded in this area: the Mediterranean horseshoe bat Rhinolophus euryale, the greater horseshoe bat R. ferrumequinum, the Mehely's horseshoe bat R. mehelyi and the Geoffroy's bat Myotis emarginatus. Considering the already well-known diffusion of the Schreibers' bat Miniopterus schreibersi, the common pipistrelle, Pipistrellus pipistrellus, the lesser mouse-eared bat Myotis blythi and the greater mouse-eared bat Myotis myotis, these new records raise to 8 the species of bats known for the region. The mammalians' checklist of the Khroumiria region includes 27 species.

Dietary composition and echolocation call design of three sympatric insectivorous bat species from China

AbstractStudying the diet of echolocating, insectivorous bats can provide important insights into their foraging behaviors and ecological constraints they are facing. By examining an extensive data set covering a period of 2 years, the present study identifies the dietary composition of three sympatric insectivorous bat species in rural areas of Beijing municipality. Each species clearly has different preferences for particular food items. Greater horseshoe bats, Rhinolophus ferrumequinum, preferred to catch nocturnal, actively flying insects, mostly moths (Lepidoptera), and to a lesser percentage flies (Diptera), beetles (Coleoptera), and flying ants and termites (Hymenoptera). Other nocturnal insects which do not exhibit any perceptible wing movements, such as true bugs (Homoptera), or strictly diurnal insects that hardly ever fly in the dark, such as grasshoppers (Orthoptera) and dragon‐ and damselflies (Odonata), were never found in droppings of horseshoe bats. Large mouse‐eared bats, Myotis chinensis, preferentially glean relatively large terrestrial prey of the order Coleoptera (mostly carabid beetles) and Orthoptera, whereas greater tube‐nosed bats, Murina leucogaster, consume predominantly smaller, diurnal Coleoptera (mostly soldier beetles, Cantharidae, and ladybugs, Coccinellidae). Our findings also indicate previously not described, significant spectro‐temporal differences in the echolocation signals of M. chinensis and M. leucogaster. The results suggest that in our study area the dramatic differences in the dietary composition of these three bat species are mainly based upon differences in their foraging behaviors, including differences in their echolocation signal structure. The dietary data provide important background information for conservational efforts, such as habitat protection.

Notes on two species of horseshoe bats, Rhinolophus ferrumequinum and R. euryale (Rhinolophidae, Chiroptera), from northern Syria

Two species of horseshoe bats (Rhinolophus ferrumequinum and R. euryale) were found roosting together at a historic site in Salaheddin Citadel, 30 km east of Lattakia, in the coastal region of northern Syria. The Greater Horseshoe Bat R. ferrumequinum constituted 63.6% of the collected specimens, while the Mediterranean Horseshoe bat R. euryale formed 36.3%. External, dental and cranial characters are discussed, measurements for the collected specimens are given; additionally, the skull structure for both species is illustrated.

Mate fidelity and intra-lineage polygyny in greater horseshoe bats

Mating strategies that lead to increased kinship within socially cooperative groups may offer inclusive fitness benefits to individuals, but can also result in higher levels of inbreeding. Here we show in a sexually segregated bat species that females avoid this conflict through two mating behaviours. First, most females revisit and breed with specific, individual males across years, so that their single offspring born in different years are full siblings. Second, relatives in the maternal line, including mothers and daughters, share breeding partners (intra-lineage polygyny) more often than expected by chance. Although these behaviours increased levels of co-ancestry among colony members, there was no concomitant rise in inbreeding. We suggest that when females engage in mate fidelity and intra-lineage polygyny, kin ties among female roost mates will be strengthened, thereby potentially contributing to social group cohesiveness. Our findings reveal the hidden complexity that can underlie polygynous breeding, and highlight a new potential route by which female mate choice could influence social evolution.

Aerial deposition of cadmium before and after the closure of an oil-fired power station in the vicinity of two nursery roosts of Rhinolophus ferrumequinum (Chiroptera, Rhinolophidae)

Aerial deposition of cadmium has been monitored from 1994-1995 to the present by extraction of cadmium from petroleum jelly coated onto ceramic tiles placed near two nursery roosts and in the foraging area of greater horseshoe bats, Rhinolophus ferrumequinum. The mean cadmium deposit from aerial precipitation recorded in the area from 1994-1995 at locations which were upwind of the power station was 0.11 ± 0.05 mg/kg/mm rain per day compared with 1.01 ± 1.60 mg/kg/mm rain per day at locations downwind. After the oil-fired power station closed in 1996 subsequent analysis from 1998-2000 showed a slight increase in cadmium precipitation at upwind locations (0.22 ± 0.06 mg/kg/mm rain per day) but a decrease at the downwind locations (0.32 ± 0.07 mg/kg/mm rain per day). After closure of the oilfired power station near the bat roosts the aerial deposition of cadmium downwind was reduced but continued monitoring of the cadmium precipitation in the area is indicated since cadmium deposition still occurs. The deposits of cadmium have not had a major impact on the number of adult bats which have increased from 1994 to 2000. The findings made in this study have implications for conservation of the greater horseshoe bats which are at the Northern limit of their distribution.

Torpor, arousal and activity of hibernating Greater Horseshoe Bats (Rhinolophus ferrumequinum)

Abstract1. Patterns of torpor, arousal and activity in free‐living Greater Horseshoe Bats, Rhinolophus ferrumequinum (Schreber), were investigated during the hibernation period by using temperature‐sensitive radio‐transmitters.2. Torpor bouts varied between 0·1 and 11·8 days, with individual means ranging from 1·3 to 7·4 days. Torpor bout duration decreased with increasing ambient temperature.3. Activity duration varied from 37 min to 54 h 24 min, with individual means ranging from 2 : 29 to 8 : 58 h. Activity duration increased with ambient temperatures above approximately 10 °C.4. Ten of 11 bats synchronized their arousals with dusk. The circadian rhythm of one bat showed a free‐running pattern over a period of about 5 weeks. Arousals were more highly synchronized, and closer to dusk, in individuals with lower body condition.5. That bats forage in mild weather is supported by the strong synchronization of arousals with dusk, especially in bats with low body condition.6. Patterns of torpor and subsequent activity are consistent with predictions that torpor lasts until a critical metabolic or water imbalance is achieved. Because metabolism and water loss are temperature‐dependent, torpor bout duration decreases with increasing temperature. The imbalance is corrected during subsequent activity, which is relatively constant in duration until a temperature threshold of 10 °C, above which increasing levels of foraging lead to longer activity bouts.

Characterization of microsatellite loci in the greater horseshoe bat Rhinolophus ferrumequinum

Characterization of microsatellite loci in the greater horseshoe bat <i>Rhinolophus ferrumequinum</i>

Nature and origin of cerebrovascular nerves with substance P immunoreactivity in bats (Mammalia: Microchiroptera), with special reference to species differences

Double staining immunohistochemistry was used to investigate the origin and projection of nerves with substance P (SP) immunoreactivity (-IR) in the walls of the major cerebral arteries in two microchiropteran species. In the greater horseshoe bat, most of the cerebral perivascular nerves with SP-IR did not exhibit calcitonin gene-related peptide (CGRP)-IR, but emitted bright immunofluorescence for vasoactive intestinal polypeptide (VIP). In this species, a large number of cell bodies with both SP- and VIP-IR were observed in many cranial ganglia along various branches of the facial and glossopharyngeal nerves. There were no cell bodies immunoreactive for either SP and VIP in the two sensory (trigeminal and upper cervical dorsal root), two sympathetic (superior cervical and stellate), or two vagal (superior and jugular) ganglia. In addition, several thick fiber bundles with both SP- and VIP-IR were present in the wall of the cerebral carotid artery, and descended progressively reaching as far as the middle part of the basilar artery (BA). These and other findings suggest that SP-immunoreactive nerves with VIP-IR but not CGRP-IR, which contribute to the rich innervation of the vertebrobasilar system in the greater horseshoe bat, originate from neurons with the same combination of peptide-IR in the major or local facial or glossopharyngeal parasympathetic ganglia, and enter the cranial cavity along the internal carotid artery. In the bent-winged bat, however, cerebral perivascular SP-immunoreactive nerves, as well as SP-immunoreactive neurons within the trigeminal and upper cervical dorsal root ganglia (uCDRG), showed neither CGRP-IR nor VIP-IR, and were mostly confined to the caudal BA and the vertebral artery (VA). These observations, in addition to the projection of this nerve type to the BA via the VA as fiber bundles, or through the meninges, indicate that the principal source of the cerebrovascular SP-immunoreactive innervation in this species is the uCDRG.