Bat wing morphology is considered in relation to flight performance and flight behaviour to clarify the functional basis for eco-morphological correlations in flying animals. Bivariate correlations are presented between wing dimensions and body mass for a range of bat families and feeding classes, and principal-components analysis is used to measure overall size, wing size and wing shape. The principal components representing wing size and wing shape (as opposed to overall size) are interpreted as being equivalent to wing loading and to aspect ratio. Relative length and area of the hand-wing or wingtip are determined independently of wing size, and are used to derive a wingtip shape index, which measures the degree of roundedness or pointedness of the wingtip. The optimal wing form for bats adapted for different modes of flight is predicted by means of mechanical and aerodynamic models. We identify and model aspects of performance likely to influence flight adaptation significantly; these include selective pressures for economic forward flight (low energy per unit time or per unit distance (equal to cost of transport)), for flight at high or low speeds, for hovering, and for turning. Turning performance is measured by two quantities: manoeuvrability, referring to the minimum space required for a turn at a given speed; and agility, relating to the rate at which a turn can be initiated. High flight speed correlates with high wing loading, good manoeuvrability is favoured by low wing loading, and turning agility should be associated with fast flight and with high wing loading. Other factors influencing wing adaptations, such as migration, flying with a foetus or young or carrying loads in flight (all of which favour large wing area), flight in cluttered environments (short wings) and modes of landing, are identified. The mechanical predictions are cast into a size-independent principal-components form, and are related to the morphology and the observed flight behaviour of different species and families of bats. In this way we provide a broadly based functional interpretation of the selective forces that influence wing morphology in bats. Measured flight speeds in bats permit testing of these predictions. Comparison of open-field free-flight speeds with morphology confirms that speed correlates with mass, wing loading and wingtip proportions as expected; there is no direct relation between speed and aspect ratio. Some adaptive trends in bat wing morphology are clear from this analysis. Insectivores hunt in a range of different ways, which are reflected in their morphology. Bats hawking high-flying insects have small, pointed wings which give good agility, high flight speeds and low cost of transport. Bats hunting for insects among vegetation, and perhaps gleaning, have very short and rounded wingtips, and often relatively short, broad wings, giving good manoeuvrability at low flight speeds. Many insectivorous species forage by `flycatching' (perching while seeking prey) and have somewhat similar morphology to gleaners. Insectivorous species foraging in more open habitats usually have slightly longer wings, and hence lower cost of transport. Piscivores forage over open stretches of water, and have very long wings giving low flight power and cost of transport, and unusually long, rounded tips for control and stability in flight. Carnivores must carry heavy loads, and thus have relatively large wing areas; their foraging strategies consist of perching, hunting and gleaning, and wing structure is similar to that of insectivorous species with similar behaviour. Perching and hovering nectarivores both have a relatively small wing area: this surprising result may result from environmental pressure for a short wingspan or from the advantage of high speed during commuting flights; the large wingtips of these bats are valuable for lift generation in slow flight. The relation between flight morphology (as an indicator of flight behaviour) and echolocation is considered. It is demonstrated that adaptive trends in wing adaptations are predictably and closely paralleled by echolocation call structure, owing to the joint constraints of flying and locating food in different ways. Pressures on flight morphology depend also on size, with most aspects of performance favouring smaller animals. Power rises rapidly as mass increases; in smaller bats the available energy margin is greater than in larger species, and they may have a more generalized repertoire of flight behaviour. Trophic pressures related to feeding strategy and behaviour are also important, and may restrict the size ranges of different feeding classes: insectivores and primary nectarivores must be relatively small, carnivores and frugivores somewhat larger. The relation of these results to bat community ecology is considered, as our predictions may be tested through comparisons between comparable, sympatric species. Our mechanical predictions apply to all bats and to all kinds of bat communities, but other factors (for example echolocation) may also contribute to specialization in feeding or behaviour, and species separation may not be determined solely by wing morphology or flight behaviour. None the less, we believe that our approach, of identifying functional correlates of bat flight behaviour and identifying these with morphological adaptations, clarifies the eco-morphological relationships of bats.

Ecological Morphology and Flight in Bats (Mammalia; Chiroptera): Wing Adaptations, Flight Performance, Foraging Strategy and Echolocation

We studied the echolocation and hunting behavior of three aerial insectivorous species of bats (Vespertilionidae: Pipistrellus) in the field in order to characterize the signals used by the bats and to determine how call structure varies in relation to habitat structure (“uncluttered” versus “cluttered” space). We documented free-flying, naturally foraging wild pipistrelles in various habitats using multiflash stereophotography combined with simultaneous sound recordings. Then we reconstructed the bat's flight position in three-dimensional space and correlated it with the corresponding echolocation sequences. In all three species of pipistrelles, signal structure varied substantially. In echolocation sequences of the search phase we found a consistent association of signal types with habitat types. In uncluttered habitats (obstacles more than 5 m from the bat) pipistrelles emitted almost exclusively narrowband signals with bandwidths less than 15 kHz. In cluttered habitats (obstacles less than 5 m from the bat) they switched to signals with bandwidths of more than 15 kHz. Wideband signals were also used when the bats were turning in cluttered and uncluttered spaces and for an instant after turning away from obstacles. Prey detection occured only when the outgoing signal did not overlap with the returning echo from potential prey. The bats also avoided overlap of echoes from potential prey and obstacles. Based on the results of this study, we propose an overlap-free “window” within which pipistrelles may detect potential prey and which allows predictions of minimum distances to prey and clutter-producing objects.

Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection

The results of recent studies of the foraging behaviour of animal-eating bats are considered in this review. The advent of small (< 1 g) radio transmitters has made it possible to collect data on i...

The foraging behaviour and ecology of animal-eating bats

The types of echolocation signal and the auditory capacities of echolocating bats are adapted to specific acoustical constraints of the foraging areas. Bats hunting insects above the canopy use low frequencies for echolocation; this is an adaptation to prey detection over long distances. Bats foraging close to and within foliage avoid masking of insect echoes by specializing on 'fluttering target' detection. 'Gleaning' bats are adapted to the auditory detection of very faint noises generated by ground-dwelling prey, and are capable of analysing fine changes in the echo spectrum, which may indicate a stationary prey changing its posture on a substrate. This review of recent research demonstrates that, in bats, foraging ecology and audition are intricately interrelated and interdependent.

Foraging ecology and audition in echolocating bats.

Echolocation signals were recorded from big brown bats, Eptesicus fuscus, flying in the field and the laboratory. In open field areas the interpulse intervals (IPI) of search signals were either around 134 ms or twice that value, 270 ms. At long IPI's the signals were of long duration (14 to 18-20 ms), narrow bandwidth, and low frequency, sweeping down to a minimum frequency (Fmin) of 22-25 kHz. At short IPI's the signals were shorter (6-13 ms), of higher frequency, and broader bandwidth. In wooded areas only short (6-11 ms) relatively broadband search signals were emitted at a higher rate (avg. IPI= 122 ms) with higher Fmin (27-30 kHz). In the laboratory the IPI was even shorter (88 ms), the duration was 3-5 ms, and the Fmin 30- 35 kHz, resembling approach phase signals of field recordings. Excluding terminal phase signals, all signals from all areas showed a negative correlation between signal duration and Fmin, i.e., the shorter the signal, the higher was Fmin. This correlation was reversed in the terminal phase of insect capture sequences, where Fmin decreased with decreasing signal duration. Overall, the signals recorded in the field were longer, with longer IPI's and greater variability in bandwidth than signals recorded in the laboratory.

Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory.

Sympatrically living echolocating bat species search for prey in different foraging zones. Structure of echolocation calls and audition are adapted to the specific foraging areas and hunting behaviors. Long pure-tone and narrow-band echolocation signals are described as adaptations to long-range echolocation and to fluttering-insect detection in echo cluttering environments. Echolocation with brief broadband signals is discussed in context with target texture discrimination and range finding by measuring echo travel times. I n the history of mammalian evolution the bats (Chiroptera) provide an impressive story of success. The well preserved fossiles from Grube Messel near Darmstadt and from Wyoming, USA tell us that already in the wake of mammalian development, some 50-60 million years ago, bats had achieved a status of sophisticated design as perfect as in recent species. Chiroptera ramified into more than 900 different species indicating that they enjoyed a niche of living little impaired by competitors from other mammalian stock or vertebrate phyla. Bats owe this flourishing existence to two unique specializations: they extended foraging on insects from the ground and vegetation into the air by developing wings and escaped the strong predatory impact of the faster flying birds by restricting their foraging flights to the night. This they could achieve because they integrated vocalization and audition into an effective echolocation system [1]. Echolocating bats emit brief sounds of high frequencies (15-200 kHz) through the mouth or the nostrils and listen to the echoes reflected from prey and objects around them. Due to the limited energy available in emitted sounds and sound absorption in air echolocation only operates over shorter distances of maximally 30-40 meters. The information from the echoes provides the bat with an auditory representation of its surroundings precise and good enough to do without any visual information. Thus unlike owls echolocating bats skillfully fly and catch prey in complete darkness [2]. Echolocation has most probably evolved in context with catching flying insects which is illustrated by the fact that all but one genus of the frugivorous Megachiroptera do not echolocate at all, but instead feature excellent night vision. Even though some echolocating bats have specialized on eccentric food like pollen, fish, frogs or warm blood most species feed on insects. In this report I shall focus the discussion on the insect-eating species. Sound recordings from about 150 of the more than 600 echolocating bat species have disclosed that the structure of echolocation pulses are widely diverse (e.g. [3-6], and many others). The frequency of the main energy emitted may range from 17 kHz to over 200 kHz and sound duration may vary from 0.3 to 200 ms. Echolocation pulses might be brief frequency-downward-modulated sweeps (FM) consisting of one to several harmonics which broaden the frequency band of the signal to up to 120 kHz. In other species, notably horseshoe bats and hipposiderids, sounds consist of combinations of long pure tones, so-called constant-fre-

G. Neuweiler

Papers

Foraging, echolocation and audition in bats