Echolocation in the notch-eared bat,Myotis emarginatus

Summary In Myotis emarginatus, the patterns of echolocation sounds vary with different foraging habitats: In commuting flights the echolocation sounds are linearly frequency modulated sweeps that start at about 100 kHz, terminate at 40 kHz, and have a duration of 1–3 ms. They consist of a loud first harmonic. The second and third harmonics are at least 15 dB fainter than the first one and often undetectable. A distinctly different type of sound is emitted when the bats search for flying insects in open spaces. The sounds are reduced in bandwidth and elongated by a constant frequency component that follows the initial frequency modulated part. Typically, sounds start at about 94 kHz and terminate in a constant frequency component at about 40–45 kHz. The average duration of the constant frequency tail is 2.8 ms; this approximately doubles the length of the pulse, with the longest recorded sound lasting 7.2 ms. When bats are foraging near and within foliage, and gleaning prey from foliage, echolocation sounds are brief (average 1 ms) frequency modulated pulses with a broad bandwidth. The pulses start at about 105 kHz and sweep down to 25 kHz. During gleaning within a building, the frequency range of the sounds is shifted to higher frequencies and extends from 124 to 52 kHz. When the bats forage for aireal insects in a confined area that creates echo-clutter, they emit sounds similar to those used during gleaning within buildings except that sound durations are extended to about 1.8 ms. In each foraging area, the echolocation sounds emitted during the search for and approach to prey are similar in structure. Sound and pause durations are reduced in the approach phase. Irrespective of foraging style and habitat, immediately before capture the bat emits a rapid and stereotyped sequence of 2-10 echolocation pulses (final buzz). These pulses are brief (0.2–0.5 ms), frequency modulated sounds with a reduced bandwidth. The sounds start at 45 kHz and sweep down to 35–20 kHz. The repetition rate is increased up to 200 pulses/s. Offprint requests to: G. Neuweiler     

Social behavior of the little brown bat,Myotis lucifugus

Behavioral Ecology and Sociobiology -     

The echolocation and hunting behavior of Daubenton's bat,Myotis daubentoni

Summary The echolocation and hunting behavior of Daubenton's bat (Myotis daubentoni) were studied in the field under completely natural conditions using a multiflash photographic system synchronized with high-speed tape recordings. The hunting behavior of M. daubentoni is separated into four stages. In the search flight stage Daubenton's bat flies with an average speed of 3.4±0.6 m/s SD usually within 30 cm over water surfaces searching for insects. After the detection of potential prey, the approach flight stage occurs, during which the bat approaches the target in a goal-directed flight. The stage tail down indicates that M. daubentoni is close to the potential prey (approximately 10–22 cm) and is preparing for the catch. The insects are caught with the interfemoral membrane, the feet, and sometimes with the additional aid of a wing. In the stage head down, the bat seizes the prey during flight. Immediately afterwards, Daubenton's bat returns to search flight. M. daubentoni shows the typical echolocation behavior of a vespertilionid bat, emitting frequency-modulated (FM) echolocation signals. The three behavioral stages search, approach, and terminal phase (Griffin et al. 1960) are used to describe the pulse pattern of foraging M. daubentoni in the field. The terminal phase (or buzz) of Daubenton's bat is separated into two parts: buzz I and buzz II. Buzz II is distinguished from buzz I by the following characteristics: a sharp drop in terminal frequency, a distinct reduction in the bandwidth of the first harmonic, a continuous high repetition rate throughout the phase in the range 155–210 Hz, very short pulses (0,25–0.3 ms) and interpulse intervals (4.5–5.0 ms) at the end of the phase, and a distinct decrease in duty cycle. A pause in echolocation separates the end of the terminal phase from the ongoing search phase. The reduction in sound duration after the detection of a target and during pursuits with successfull or attempted catches is discussed in relation to the actual distance of the bat to the target at each stage. It is likely that Daubenton's bat reduces sound duration during approach and terminal phase in order to prevent an overlap of an outgoing pulse with the returning echo from the target. It is argued that the minimum detection distance can be estimated from the sound duration during search flight. Estimates of detection and reaction distances of M. daubentoni based upon synchronized photos and echolocation sequences are given to corroborate this hypothesis. An average detection distance of 128 cm and an average reaction distance of 112 cm were determined. Each behavioral stage of foraging M. daubentoni is characterized by a distinct pattern of echolocation signals and a distinct stage in hunting behavior. The approach flight in hunting behavior coincides with the approach phase and with buzz I in echolocation behavior. The stage tail down corresponds to buzz II. The stage head down is correlated with a pause in echolocation. Immediately afterwards, the bat returns into search flight and into the search phase, emitting search signals.     

Differences in sensory ecology contribute to resource partitioning in the bats Myotis bechsteinii and Myotis nattereri (Chiroptera: Vespertilionidae)

Coexisting animal species frequently differ in resource use in at least one niche dimension and thus avoid competition. While a range of morphological differences that lead to differentiation in animals' mechanical access to food have been identified, the role of sensory differences in within-guild niche differentiation has received less attention. We tested the hypothesis that differences in sensory access to prey contribute to resource partitioning between potentially competing species using two sympatric, similar-sized, congeneric bat species as a model system. Nursery colonies of Natterer's bat (Myotis nattereri) and Bechstein's bat (Myotis bechsteinii) roost in bat boxes in the same orchard and forage in forests and orchards nearby. In observations and behavioural experiments with freshly captured M. bechsteinii, we showed that individuals are able to hunt using prey-generated sound alone. In contrast, M. nattereri rarely uses prey-generated sound, but instead is able to find prey by echolocation very close to vegetation. In accordance with these behavioural data, we showed that M. bechsteinii has significantly larger ears than M. nattereri, providing it with superior detection and localization abilities for relatively low-frequency prey rustling sounds. We hypothesized that these differences in sensory ecology of the two syntopic, congeneric species would contribute to resource partitioning, so that M. bechsteinii would find more noisy prey taxa, possibly hidden in vegetation, by listening for prey sounds, while M. nattereri would have better access to still prey using echolocation or associative learning. Analysis of faecal samples collected on the same nights from bat boxes occupied by each species corroborated this prediction. The diets of the two species differed significantly, reflecting their different prey perception techniques and thereby supporting the hypothesis that differences in sensory ecology contribute to niche differentiation. Electronic supplementary material Supplementary material is available for this article at and accessible for authorised users. B.M. Siemers and S.M. Swift contributed equally to this work.     

Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats (Rhinolophus ferrumequinum) exhibit strong natal philopatry to their maternity roost over many years, leading to the aggregation of matrilineal kin. Maternity colonies may, therefore, be expected to comprise highly related individuals, and, as such, provide conditions suitable for the evolution of kin-selected behaviours. To test these predictions, we examined relatedness and behaviour among matrilineal kin within a colony in south-west Britain. Genetic analysis of 15 matrilines, identified from microsatellite genotyping and long-term ringing surveys, revealed average relatedness levels of 0.17 to 0.64. In contrast, background relatedness among colony females approximated to zero (0.03). These results suggest that inclusive fitness benefits may only be accrued through discriminate cooperation within matrilines, and not at the wider colony level. To examine whether the potential for such benefits is realised through kin- biased cooperation during foraging, females from two matrilines were radio-tracked simultaneously over 3 years. Pairwise home-range overlap correlated significantly with Hamilton's relatedness coefficient. The greatest spatial associations were observed between females and their adult daughters, which shared both foraging grounds and night roosts, sometimes over several years. Tagged females, however, generally foraged and roosted alone, suggesting that kin-biased spatial association probably does not result from either information-transfer or cooperative territorial defence. Such patterns may instead result from a mechanism of maternal inheritance of preferred foraging and roosting sites.     

Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka

Summary In October 1984 foraging areas and foraging behaviour of the rufous horseshoe bat, Rhinolophus rouxi, were studied around a nursery colony on the hill slopes of Sri Lanka. The bats only foraged in dense forest and were not found in open woodlands (Fig. 1). This strongly supports the hypothesis that detection of fluttering prey is by pure tone echolocation within or close to echo-cluttering foliage. During a first activity period after sunset for about 30–60 min, the bats mainly caught insects on the wing. This was followed by a period of inactivity for another 60–120 min. Thereafter the bats resumed foraging throughout the night. They mainly alighted on specific twigs and foraged in flycatcher style. Individual bats maintained individual foraging areas of about 20x20 m. They stayed in this area throughout the night and returned to the same area on subsequent nights. Within this area the bats generally alighted on twigs at the same spots. Foraging areas were not defended against intruders. The bats echolocated throughout the night at an average repetition rate of 9.6±1.4 sounds/s. While hanging on twigs they scanned the surrounding area for flying prey by turning their bodies continuously around their legs. On average they performed one brief catching flight every 2 min and immediately returned to one of their favourite vantage points. Echolocation sounds may consist of up to three parts, a brief initial frequency-modulated (FM) component, a long constant frequency (CF) part lasting for about 40–50 ms, and a final FM part again (Fig. 4b, c). Adult males and females emitted pure tone frequencies in separate bands, the males from 73.5–77 kHz and the females from 76.5–79 kHz (Fig. 5). During scanning for prey from vantage points, the bats mostly emitted pure tones without any FM component (Fig. 4a). The last few pure tones emitted before take-off were prolonged to about 60 ms duration. The final FM part was therefore not an obligatory component of the echolocation signals in horseshoe bats. During flight and especially during emergence from the cave, most sounds consisted of a pure tone and loud initial and final FM sweeps. We therefore suggest that the initial FM part might also be relevant for echolocation. From our observations we conclude that the FM components are especially important during obstacle avoidance. In most sounds emitted in the field a fainter first harmonic was present. It was usually up to 30 dB fainter than the second harmonic, but in some instances it was as loud or even distinctly louder than the second one (Fig. 6a). Even within one sound the intensity relationship between the two harmonics may be reversed. We therefore suggest that the first harmonic is an integral part of the signal and relevant for information analysis in echolocation.     

Aggregation and foraging behavior of whirligig beetles (Gyrinidae)

Summary Whirligig beetles aggregate in the daytime into dense single-and multispecies groups (rafts) of hundreds or thousands of individuals. On the 22km shoreline of Lake Itasca in northern Minnesota, these aggregations were on the average 0.8 km apart, and they were usually found day after day in the same ocations.Most beetles apparently do not home to the aggregation of their origin after dispersing at night because (a) the species composition of some aggregations changed greatly, and (b) paint-marked beetles (Dineutus horni) moved overnight from one aggregation as far as 4km, joining 11 of the 14 large (>300 beetles) D. horni groups on the lake.Throughout the night, the largest concentrations of beetles remained within 100m of the diurnal aggregation sites. Beetles reconvened into the compact rafts before daybreak, in part by following each other in sometimes long single files or trains. Their forward motion stopped after they joined large number of other beetles. We infer that following behavior enables those individuals that have dispersed from their original aggregations (during their nocturnal foraging) to find and join other aggregations before daylight.Naive fish ate the beetles despite their noxious secretions. However, fish living near rafting sites and feeding on insects on the water surface in daylight should soon learn to avoid the beetles. The rafting sites would then become safe places. We observed fish attacking only those beetles that had been either dispersed from their rafts or released into open water away from raft sites in the daytime. We speculate that the evolutionary significance of the aggregation behavior is related to predator (fish) avoidance.     

Inter- and intra-year variation in foraging areas of breeding kittiwakes (Rissa tridactyla)

While seabird conservation efforts have largely focused on protection from threats at the colony (e.g. reducing disturbance and predation), attention is increasingly being given to implementing protection measures for foraging areas at sea. For this to be effective, important foraging areas must be identified. Although numerous studies have examined seabird foraging behaviour, information is still lacking on the variability in area utilisation within and among breeding seasons. GPS devices were attached to adult black-legged kittiwakes breeding at an expanding North Sea colony (55°20′N, 1°32′W) during both incubation and chick-rearing in 2012 and during chick-rearing in 2011, to determine whether foraging areas remained consistent and to identify the oceanographic characteristics of areas used for foraging. The type and size of prey items consumed at different stages of the breeding cycle was also examined. During incubation (April–May 2012), kittiwakes foraged substantially further from the colony and fed on larger sandeels than when feeding chicks, and there was significant inter-annual variation in foraging areas used during the chick-rearing period (June–July 2011 and 2012). Foraging areas were characterised by cooler sea surface temperatures and areas of high chlorophyll a concentration, although association with specific oceanographic features changed within the breeding season and between years. These results emphasise the importance of considering how foraging areas and reliance on specific oceanographic conditions change over time when seeking to identify important marine areas for seabirds.     

Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii)

In order to understand why animals are social and how group members interact with each other it is important to know their relatedness. However, few studies have investigated the genealogy in complete social groups of free-living animals with low reproductive skew. This holds particularly true for bats. Although almost all bat species are social, their sociobiology is not well understood. Because they are volant, nocturnal and have a rather cryptic life-style, bats are difficult to observe in the wild. Furthermore females are generally gregarious making genetic parent-offspring assignment a challenging task. We used genetic markers in combination with knowledge about age and colony membership of individually marked bats to construct pedigrees in completely sampled maternity colonies of Bechstein's bats (Myotis bechsteinii). Despite considerable fluctuations in population size, no immigration occurred over 5 years in four colonies living in close proximity. Additionally, confrontation tests showed that females of one maternity colony were able to detect and attempted to prevent the intrusion of foreign females into a roost they occupy. Although colonies were absolutely closed, and 75% of the colony members lived together with close relatives (rS=0.25), mean colony relatedness was nearly zero (0.02). Average relatedness therefore is a poor estimator for the potential of kin selection in Bechstein's bat colonies and may be misleading when attempting to understand the social structure of animals living in groups where many members breed. Based on our results we discuss the potential adaptive value of living in closed societies with low reproductive skew.     

Prey detection in trawling insectivorous bats: duckweed affects hunting behaviour in Daubenton's bat, Myotis daubentonii

Daubenton's bat, a trawling vespertilionid bat species, hunts for insects that fly close to, or rest on, the water surface. During summer, many ponds at which Daubenton's bats hunt become gradually covered with duckweed. The purpose of this study was to investigate the effects of duckweed cover on the hunting behaviour of Daubenton's bats and on the ultrasound-reflecting properties of the water surface. Our study revealed the following. (1) Daubenton's bat avoids water surfaces covered with duckweed. (2) Prey abundance was related to the number of foraging Daubenton's bats but was independent of duckweed cover. (3) When mealworms were presented among standardized amounts of duckweed to naturally foraging Daubenton's bats, they caught significantly less mealworms when the duckweed cover was increased. (4) Measurements with ultrasonic signals show that a water surface covered with duckweed returns a much stronger background echo at small angles (i.e. parallel to the water surface) compared to an uncovered water surface. It seems likely that a cover of duckweed on the water surface interferes with prey detection by masking the echoes returning from prey. (5) It was relatively difficult for the bats to discriminate small patches of duckweed from mealworms. The proposed discrimination mechanism for this trawling bat species suggests that single duckweed patches can also be mistaken for natural prey by Daubenton's bats. Received: 4 January 1998 / Accepted after revision: 19 July 1998     

Foraging behavior and echolocation of wild horseshoe bats Rhinolophus ferrumequinum and R. hipposideros (Chiroptera,Rhinolophidae)

Summary 1. Echolocation and foraging behavior of the horseshoe bats Rhinolophus ferrumequinum and R. hipposideros feeding under natural conditions are described. 2. The calls of both species consisted predominantly of a long CF segment, often initiated and terminated by brief FM sweeps of substantial bandwidth. 3. R. hipposideros typically flew close to vegetation, and fed by aerial hawking, gleaning and by pouncing on prey close to the ground. R. hipposideros called with a CF segment close to 112 kHz which is the second harmonic of the vocalization; its calls included low intensity primary harmonics, and had prominent initial and terminal FM sweeps of considerable bandwidth. When searching for prey on the wing it had longer interpulse intervals than R. ferrumequinum, but emitted shorter pulses at a higher repetition rate; overall it had a similar duty cycle to R. ferrumequinum. 4. R. ferrumequinum, calling with a CF segment close to 83 kHz, also used harmonics other than the dominant secondary in its calls, and modified its echolocation according to ecological conditions. This species showed certain parallels with R. rouxi of Asia. It was observed feeding by aerial hawking and by flycatching. When scanning for prey from a perch (perch hunting), calls were of shorter duration, and interpulse intervals were on average longer, than when bats were flying. Mean duty cycle was longer in flight, and the bandwidths and frequency sweep rates of the FM segments in the calls increased in comparison with perched bats. 5. FM information may facilitate determination of target range and the location and nature of obstacles; it may also be involved in the interpretation of echoes and the detection of moving targets among clutter. The rising FM sweep initiating the call in both species when flying (and to a lesser extent perch hunting) in the wild must have a significant adaptive role, and should be considered an essential component of the call; rhinolophids should be termed FM/CF/FM bats.Abbreviations CF constant frequency - FM frequency modulated - FM₁ initial rising frequency sweep - FM₂ terminal falling frequency sweep - PRR pulse repetition rate - SD standard deviation - SNR signal-to-noise ratio     

Foraging habitat and echolocation behaviour of Schneider's leafnosed bat, Hipposideros speoris, in a vegetation mosaic in Sri Lanka

The Hipposideridae and Rhinolophidae are closely related families of bats that have similar echolocation (long-duration pure-tone signal, high duty cycle) and auditory systems (Doppler-shift compensation, auditory fovea). Rhinolophid bats are known to forage in highly cluttered areas where they capture fluttering insects, whereas the foraging habitat of hipposiderid bats is not well understood. Compared to rhinolophids, hipposiderid calls are shorter in duration, have lower duty cycles, and they exhibit only partial Doppler-shift compensation. These differences suggest that the foraging habitat of the two families may also differ. We tested this hypothesis by studying foraging and echolocation of Hipposideros speoris at a site with a range of vegetation types. Bats foraged only while in flight and used all available closed and edge habitats, including areas adjacent to open space. Levels of clutter were high in forest and moderate in other foraging areas. Prey capture (n=42) occurred in edge vegetation where it bordered open space. Echolocation signals of H. speoris lacked an initial upward frequency-modulated sweep and were of moderate duration (5.1-8.7 ms). Sequences had high duty cycles (23-41%) and very high pulse repetition rates (22.8-60.6 Hz). Variation in signal parameters during search phase flight across foraging habitats was low. H. speoris showed a greater flexibility in its use of foraging habitat than is known for any rhinolophid species. Our study confirmed that there are differences in habitat use between hipposiderid and rhinolophid bats and we suggest that this divergence is a consequence of differences in their echolocation and auditory systems.     

Fishing and echolocation behavior of the greater bulldog bat,Noctilio leporinus,in the field

When hunting for fish Noctilio leporinus uses several strategies. In high search flight it flies within 20–50 cm of the water surface and emits groups of two to four echolocation signals, always containing at least one pure constant frequency (CF) pulse and one mixed CF-FM pulse consisting of a CF component which is followed by a frequency-modulated (FM) component. The pure CF signals are the longest, with an average duration of 13.3 ms and a maximum of 17 ms. The CF component of the CF-FM signals averages 8.9 ms, the FM sweeps 3.9 ms. The CF components have frequencies of 52.8–56.2 kHz and the FM components have an average bandwidth of 25.9 kHz. A bat in high search flight reacts to jumping fish with pointed dips at the spot where a fish has broken the surface. As it descends to the water surface the bat shows the typical approach pattern of all bats with decreasing pulse duration and pulse interval. A jumping fish reveals itself by a typical pattern of temporary echo glints, reflected back to the bat from its body and from the water disturbance. In low search flight N. leporinus drops to a height of only 4–10 cm, with body parallel to the water, legs extended straight back and turned slightly downward, and feet cocked somewhat above the line of the legs and poised within 2–4 cm of the water surface. In this situation N. leporinus emits long series of short CF-FM pulses with an average duration of 5.6 ms (CF 3.1 and FM 2.6) and an average pulse interval of 20 ms, indicating that it is looking for targets within a short range. N. leporinus also makes pointed dips during low search flight by rapidly snapping the feet into the water at the spot where it has localized a jumping fish or disturbance. In the random rake mode, N. leporinus drops to the water surface, lowers its feet and drags its claws through the water in relatively straight lines for up to 10m. The echolocation behavior is similar to that of high search flight. This indicates that in this hunting mode N. leporinus is not pursuing specific targets, and that raking is a random or statistical search for surface fishes. When raking, the bat uses two strategies. In directed random rake it rakes through patches of water where fish jumping activity is high. Our interpretation is that the bat detects this activity by echolocation but prefers not to concentrate on a single jumping fish. In the absence of jumping fish, after flying for several minutes without any dips, N. leporinus starts to make very long rakes in areas where it has hunted successfully before (memory-directed random rake). Hunting bats caught a fish approximately once in every 50–200 passes through the hunting area.     

Individual differences in foraging behavior and cortisol levels in recently emerged brook charr (Salvelinus fontinalis)

Recently emerged brook charr (Salvelinus fontinalis) foraging in still-water pools along the sides of streams tend to be either sedentary, feeding from the lower portion of the water column (a sit-and-wait tactic), or very active, feeding from the upper portion of the water column (an active search tactic). We tested whether the individual differences in foraging behavior were associated with baseline concentrations and responses of cortisol, a steroid hormone linked to personality differences in a variety of animals including fishes. We quantified the proportion of time spent on moving by focal charr in the field and then capturing them. Captured individuals were either (i) sacrificed immediately to quantify baseline cortisol concentrations, (ii) held in an unfamiliar field environment for 15 min and then sacrificed to quantify cortisol concentrations in response to handling and holding in a novel field environment, or (iii) held in an unfamiliar field environment with a white Plexiglas base (stressor) for 15 min to quantify cortisol concentrations in response to a novel object. Eleven statistical models relating cortisol concentrations to the proportion of time individuals spent on moving while searching for prey were compared using multi-model inferencing. Cortisol concentrations were higher for charr that spent a lower proportion of time on moving in the field than for charr that spent a higher proportion of time on moving. For a given proportion of time spent on moving, mean cortisol concentrations between baseline and experimental treatments, our measure of cortisol response, did not differ markedly. Our findings suggest that the foraging tactics displayed by wild brook charr in the field could reflect differences in how individuals perceive their environment.