The foraging behaviour and ecology of animal-eating bats

M. BROCKFENTON
Department of Biology, York University, North York, Ont., Canada M3J 1P3
Received February 3, 1989

FENTON, M. B . 1990. The foraging behaviour and ecology of animal-eating bats. Can. J. Zool. 68: 41 1-422.
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 individual variations in foraging behaviour for species with body
mass over 15 g. These data can be combined with those from wing morphology and echolocation call design to assess the
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flexibility achieved by some bats. The information concerning bats can be placed in a broader perspective by considering it in the
light of current ideas about foraging theory. In this review, information about bat foraging is considered in the context of
structural and functional features, the former relating to bats' access to habitats of different complexity and the latter to their
behavioural responses. Mechanical features involving wing morphology and perceptual features, such as the ability of
echolocating bats to deal with clutter, combine to influence the behavioural flexibility of individuals. This, in turn, affects access
to prey and patterns of community structure. Bats relying on airborne prey appear to be limited to small prey items, whereas those
hunting nonairborne targets may take much larger prey. Variation in individual behaviour means that terms such as gleaning,
perch hunting, piscivory, and camivory do not accurately define the foraging of animal-eating bats. Morphological and
behavioural data suggest that sympatric animal-eating bats of similar size will show considerable overlap in prey taken and in
patterns of habitat use.

FENTON, M. B. 1990. The foraging behaviour and ecology of animal-eating bats. Can. J. Zool. 68 : 41 1-422.
On trouvera ici une rkvision des rksultats d'itudes rkcentes sur le comportement de quCte de nourriture chez des chauves-souris
qui mangent des animaux. L'avknement de petits kmetteurs radio (<1 g) a rendu possible l'accumulation de donnkes sur les
variations individuelles dans le comportement de recherche de nourriture chez des espkces de masse supkrieure a 15 g. Ces
For personal use only.

donnkes, combinkes aux informations sur la morphologie des ailes et sur les cris d'kcholocation, permettent d'kvaluer la
flexibilitk de certaines chauves-souris. L'information sur les chauves-souris peut ktre considkrke dans une perspective plus vaste
a la lumikre des concepts rkcents sur la thkorie de la qukte de nourriture. Dans cette revision, l'information sur la qukte de
nourriture chez les chauves-souris est envisagke dans le contexte des caractkristiques structurales, notamment l'accks des
chauves-souris a des habitats de complexitks diverses, et des caractkristiques fonctionnelles, par exemple les rkactions
kthologiques. Des aspects micaniques reliis a la morphologie des ailes et a la perception, notamment la capacitk qu'ont les
chauves-souris qui repkrent leurs proies par kcholocation de reconnaitre les obstacles, contribuent a la flexibilitk du
comportement des individus. Ce phknomkne influence a son tour I'accks aux proies et l'allure de la structure de la communautk.
Les chauves-souris qui consomment des proies volantes semblent lirnitkes a de petites proies, alors que celles qui ont pour cibles
des proies qui ne volent pas peuvent consommer des proies beaucoup plus grosses. Les variations du comportement individuel
signifient que les termes tels que rkcolte, chasse au perchoir, piscivorisme et camivorisme, ne dkcrivent pas exactement le
comportement de qukte de nourriture des chauves-souris mangeuses d'animaux. Des donnies morphologiques et kthologiques
indiquent que, chez les chauves-souris sympatrides qui sont de tailles semblables et qui mangent des animaux, il peut y avoir un
important chevauchement des proies et des patterns d'utilisation de I'habitat.
[Traduit par la revue]

The 600 or so species of animal-eating bats are arranged in 16 some species feed on insects, others on blood, fruit, nectar and
families and represent a diverse assemblage of forms and habits pollen, or fish (e.g., Miller 1907;. Allen 1939). McNab (197 1)
(Hill and Smith 1984). There are tropical locations where more proposed that bat communities are composed of up to seven
than 50 species of animal-eating bats are sympatric, and even feeding associations: piscivory, sanguinivory, aerial insecti-
some north-temperate communities are composed of 10-15 vory, foliage-gleaning insectivory, nectarivory, frugivory, and
species. In trying to understand the factors underlying the omnivory . Other workers (e.g., Willig 1986) have referred to
radiation of these bats, workers have identified different these associations as guilds, and some have made finer
approaches to foraging, using parameters ranging from mor- distinctions among animal-eating species. For example, Hill
phology and prey selection to patterns of habitat use and mode and Smith (1984) added carnivory to this array, and among the
of orientation. As the diversity of these animals is considerable, insectivorous forms, distinguished species using "terrestrial
reflecting continua between different extremes, it is not surpris- acquisition" as a separate strategy. Norberg and Rayner (1987)
ing that the picture of bat foraging emerging from these studies used wing morphology, diet, echolocation behaviour , and
is eclectic and often conflicting. In considering access to food as patterns of habitat use as the bases for arranging insectivorous
a factor that imposes organization on the communities of bats, it bats in five categories: fast hawking, slow hawking, trawling,
is important to acknowledge that there is little evidence that food gleaning and hovering, and flycatching and perch hunting. They
is a limiting resource, at least for animal-eating bats. Roosts also also distinguished carnivorous and piscivorous bats as separate
are critical resources and may have more profound effects on bat groups. Neuweiler (1984) used patterns of habitat use to identify
communities (e.g ., Brosset 1966). three basic approaches to foraging in the southern Indian
Several workers have used food and feeding as the bases for community of animal-eating bats he studied: species working
categorizing different bats, beginning with the recognition that close to the ground, those operating close to and within
 412 CAN. J. ZOOL. VOL. 68, 1990

canopies, and those foraging in open spaces. Other published

proposals are variations on these themes (e.g., Wallin 1969;
Fenton 1982; Aldridge and Rautenbach 1987; Crome and
Richards 1988).
Variation in the behaviour of individuals probably presents
the most important challenge to proposed classifications of
foraging by animal-eating bats, and McNab (197 1) recognized
this when he identified some species as "omnivorous." Subse-
quent studies have documented the range of food in the diets of
some phyllostomine bats (e .g . , Gardner 1977; Humphrey et a1.
1983; Belwood 1988), and for these bats Willig ('1986)
questioned the clarity of the boundaries between "guilds."
Variations in diet could result from some combination of
differences in patterns of habitat use, foraging behaviour, and
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prey availability, confounding efforts to categorize animal-

eating bats by their diet or foraging behaviour.
Structural and functional components affect the foraging
FIG. 1. Diagrammatic representation of habitats available to for-
behaviour of bats, the structural component reflecting the nature aging bats, distinguishing closed habitats (cross-hatched) from edge
of the habitat and the functional component the behaviour of the (stippled) and open (clear) ones.
animals. The two components are not discrete, however, for
habitat structure affects not only bats' access to habitats
(according to their mechanical and perceptual abilities) but also obstacles that a flying bat must detect and avoid, along the
the accessible populations of their prey (including abundance, spectrum from wide open habitats to areas within the canopies
distribution, and composition). of trees and bushes. The array of obstacles is commonly referred
A model of maximum energy intake per unit time spent to as "clutter," a term from radar theory referring to echoes from
foraging (Mittelbach 1981; Werner and Mittelbach 1981) other than the target of interest. Among bat biologists, clutter is
identifies some of the data required to understand the functional a commonly used but ill-defined term. In this paper I will
approach that bats may take to hunting, and can help to put the consider clutter from the point of view of a bat searching for
For personal use only.

foraging behaviour of animal-eating bats in a broader perspec- prey, because bats that have detected and are pursuing airborne
tive. The model considers the energy intake per unit time spent prey often chase them into cluttered situations and have had the
foraging in a habitat, the assimilable portion of prey, the energy opportunity to "lock onto" their target. From the bat's perspec-
content (joules) of prey, the prey handling time (seconds), and tive, clutter presents two problems, one perceptual, the other
the energetic cost of prey handling, Ch (joules per second). The mechanical. The perceptual problem lies in detecting the echoes
energetic cost of searching for prey, C, (joules per second), and from a target amid echoes from clutter, and the mechanical one
the rate at which prey are encountered, A, also are considered. in manoeuvring to avoid collisions with obstacles.
This model differs from some optimal foraging versions (e.g., The mechanical problem may be quantifiable as the number
Werner and Hall 1974) because it includes the energetic costs of of changes in course necessary to avoid collision with obstacles
searching and foraging. The various approaches to foraging by per unit distance travelled. The distance units should be scaled
animal-eating bats are organized around differences in A, C,, according to bat size, so expressing them as body length (or
and Ch. wingspan) recognizes the inherent differences in bat flight
The purpose of this paper is to review the foraging behaviour performance attributable to size (e.g ., Aldridge and Rautenbach
of animal-eating bats, interpreting the behaviour in the context 1987; Norberg and Rayner 1987). The rate at which the bat
of the available data, and using the data to generate predictions . moves through the habitat (number of body lengths per unit
testable with bats in field or laboratory settings. The information time) and the distance (in body lengths) at which it detects
also is used to categorize the foraging of animal-eating bats different objects must be considered when measuring clutter.
around a sequence common in hunting behaviour, namely the For example, echolocating Eptesicus fuscus first detected
progression from searching to detecting, approaching and- 19 rnrn diameter spheres at 5 m (Kick 1982). When scaled, these
attacking, and consuming prey. In the first part of the review I results show that, using echolocation, an 11 cm long E. fuscus
will consider the structural (i.e., access to habitat) and function- first detects an object 17% of its total length (head, body, and
al (i.e., behavioural, including search cost, prey selection, tail) at a distance of 45 total lengths. When foraging, these bats
flexibility, and decision making) components of bat foraging. fly at about 32 total lengthsls (Brigham 1988), meaning that
Then I will examine proposals that gleaning, perch hunting, target-sized obstacles are evident 1.5 s in front of the bat. It is
carnivory, and piscivory represent different foraging strategies safe to assume that larger objects are detected at greater
of bats, before reflecting on the implications of the review for distances and that the interval between search phase echoloca-
understanding the structure of communities of animal-eating tion calls may set the maximum limits of detection (Table 1) in
bats. species intolerant of pulse-echo overlap.
The array of habitats depicted in Fig. 1 presents at least three
Structural components situations with respect to clutter (Fig. 2). In the open habitats a
Several workers have identified the various habitats available bat may expect to encounter nothing in "close" range but
to foraging bats and noted that they range from open skies to potential prey or other bats. Perceptually this means no overlap
areas within thick vegetation (Fig. 1; for example, see Wallin of echoes from targets with those from clutter. In edge habitats,
1969; Neuweiler 1984; Aldridge and Rautenbach 1987). This the orientation of its flight path may present clutter to the bat in
variety involves a progressive increase in the numbers of an orderly and predictable way, e.g., for a fishing bat (Noctilio
 TABLE1 . If echolocating bats do not tolerate overlap between the echo from one pulse and
the next pulse, the maximum range of target detection may be estimated from the interval
between pulses; the values represent the lowest rates at which some bats produce echo-
location calls while searching for prey

Interpulse
interval Range
(ms> (m> Source

Rhinopoma hardwickei Simmons et al. 1984

Taphozous mauritianus Fenton et al. 1980
Cormura brevirostris Barclay 1983
Saccopteryx bilineata Barclay 1983
Nycteris grandis Fenton et al. 1983
Nycteris thebaica Fenton et al. 1983
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Noctilio leporinus Suthers 1965

Noctilio labialis Suthers and Fattu 1973
Trachops cirrhosus Barclay et al. 1981
Myotis adversus Thompson and Fenton 1982
Myotis daubentoni Jones and Rayner 1988
Lasionycteris noctivagans Barclay 1986
Eptesicus fuscus Simmons et al. 1979
Chalinolobus variegatus Obrist et al. 1989
tasiurus cinereus Barclay 1986
Euderrna maculatum Leonard and Fenton 1984
NOTE:The rates are shown as interpulse interval (converted to range of operation, assuming that the speed of sound
inair is 340 m . s - I .
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Mechanical components: fast, agile, inexpensive flight, i.e., high aspect ratio, high wing loading, long, pointed wingtips; average
to short wingspan
Perceptual components: high-intensity, long, narrowband echolocation calls of lower frequency

CLOSED , b EDGE

Mechanical components: expensive, manoeuvrable flight, i.e., Mechanical components: slow inexpensive, manoeuvrable
low aspect ratio, low wing loading, rounded wing tips; flight, i.e., high aspect ratio, low wing loading, short,
average wingspan rounded wing tips; long wingspan
Perceptual components: plasticity in sensory behaviour, uses Perceptual components: high-intensity, shorter echolocation
echolocation or prey-generated cues or vision to find prey; calls with broadband and narrowband components; some
echolocation calls are short, low-intensity and broadband; species use a flutter-detection approach to echolocation
some species use a flutter-detection approach to echoloca-
tion

FIG. 2. Wing morphology and perceptual details of bats operating in open, edge, and closed habitats. The length of the arrows represents the
degree of flexibility potentially exhibited by bats with the mechanical and perceptual properties shown. The bat silhouettes are based on information
in Norberg and Rayner (1987), and the echolocation call features are depicted as sonograms (for details see Fig. 3).
 414 CAN. J. ZOOL. VOL. 68, 1990

leporinus) hunting over the surface of water or a sandbank.

Although the echoes from clutter overlap those from targets,
edge habitats may permit bats searching for prey to deal with
clutter in two dimensions. In closed habitats clutter generates
both perceptual and mechanical problems because bats must
deal with it in three dimensions.
Perceptual and mechanical components determine a bat's
ability to deal with clutter. Echolocation is an important part of
the perceptual component and involves the bat's tolerance for
overlap in echoes as well as its ability to simultaneously detect
and define echoes from several sources including prey and FIG. 3. Sonograms of representative echolocation calls of bats using
obstacles. The mechanical factor will be the bat's aerial flutter-detection. systems ( c , 6 ) and broadband ( a , 6 , f, g, e ) or
manoeuvrability and agility which are directly affected by wing narrowband ( h , i) signals. Species using low-intensity , short, broad-
morphology (Aldridge and Rautenbach 1987; Norberg and band signals ( a , 6 ) often rely on prey-generated cues to detect targets.
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Rayner 1987). The limits set by these two factors will restrict the Many calls (e.g., f, g, h) combine broadband and narrowband
performance of individual bats, as indicated by the arrows in components. The flutter-detecting calls are traditionally referred to as
Fig. 2, i.e., an animal's ability to deal with clutter will influence constant-frequency, frequency-modulated (CF-FM) ( c , 4, and others
as steep FM ( a , 6 ,f , e ) or combinations of steep and shallow or shallow
its access to cluttered habitats. This means that bats adapted to FM components ( h ,f , g, i).
operate in open situations will not be able to search effectively
for prey in edge or closed habitats. Those exploiting edge
habitats will have access to the open habitats but not to the (Fig. 3). Although these calls are sometimes referred to as CF
closed ones, and those adapted for closed habitats also can (see Neuweiler and Fenton 1988), they usually involve shallow
function in edge and open situations. FM sweeps that over their durations are narrow in bandwidth,
Flight dynamics reflect wing morphology and will affect the but not CF. Species foraging in edge habitats usually produce
efficiency with which different species operate in different calls that show a combination of broadband and narrowband
settings. Species with long narrow wings will have the lowest components (Fig. 3), whereas those hunting in closed habitats
costs of flight, and those with shorter, broad wings will have the usually produce short broadband calls referred to as steep FM.
For personal use only.

highest ones (Norberg and Rayner 1987). The costs of flight and Although the intensities of the echolocation calls of species
the potential rate of prey capture will directly affect the ability foraging in the open or along edges are usually high (ca. 110 dB
of bats to operate efficiently in different habitats. As morpho- sound pressure level (SPL) at 10 cm (Griffin 1958)), and those
metric studies (e.g., Findley and Wilson 1982; Schum 1984) of species operating in closed habitats are usually low (<70 dB
repeatedly demonstrate that within bat communities there is SPL at 10 cm (Griffin 1958)), there are few data on individual
general similarity between most sympatric species (quantified variation in call intensity.
as distance to nearest neighbour) and few dramatically different Bats foraging in closed habitats often use prey-generated
ones (quantified as distance to farthest neighbour), it is not sounds or visual cues to locate targets, apparently relying upon
surprising that studies of habitat use show broad overlap echolocation to collect information about their surroundings
between most sympatric forms (e.g., Bell 1980; Furlonger et al. (e.g., Fiedler 1979; Barclay et al. 1981; Tuttle and Ryan 1981;
1987). Capture studies, or those based on monitoring echoloca- Bell 1982; Fenton et al. 1983; review by Suthers and Wenstrup
tion calls, may not permit observers to document the full range 1987; Bell 1985; Ryan and Tuttle 1987). Although some of
of species' activities in different habitats (e.g., Baagoe 1987). these species may be able to use echolocation to characterize a
However, active tags (light tags or radio transmitters) often hard target on a hard background (Schmidt 1988), the use of
permit observers to find the bats and observe what they are prey-generated cues appears to be more effective. Tyrell(1988)
doing and where, providing an accurate picture of habitat use. showed how Megaderma spasma located flying targets by using
There is also overlap in the general design of search-phase prey-generated cues rather than echolocation. The low-
echolocation calls (Fig. 3), and echolocating bats use broadband intensity, short (<2 ms) broadband calls typical of closed
calls as they approach and attack targets. From an echolocation habitat foragers may minimize echoes from clutter and the
standpoint, the most distinctive bats are species in the Rhinolo- chances of alerting possible prey (Fullard 1987). The low
phidae and Hipposideridae, and the mormoopid Pteronotus intensity of the calls and the short interpulse intervals (typically
parnellii, whose auditory systems are specialized for flutter ca. 20 ms, Table 1) may combine to severely limit the effective
detection by perception of Doppler-shifted echoes. The calls of range of operation by closed habitat bats and oblige them to use
these species are dominated by constant frequency (CF) slow, expensive flight even when operating in less cluttered
components (Vater 1987) and are characterized by high duty settings.
cycles (>60%), but the calls include broadband frequency- The importance of information about prey collected other
modulated (FM) components. It is clear that this approach to than through echolocation by edge and open area foraging bats
echolocation, apparently already present in Eocene bats (Haber- remains unclear. H a m and Bailey ( 1985) demonstrated that
setzer and Storch 1987), allows the bat to use echolocation to Eptesicus fuscus learned to distinguish between the flight
identify fluttering targets against a nonfluttering background sounds of different insects, but they did not show that the bats
(Bell and Fenton 1984; Vater 1987). This is one perceptual used this information to find prey under natural conditions.
approach that permits bats to operate effectively in closed and High-intensity echolocation calls may preclude operation in
edge habitats. closed habitats because they generate a multitude of echoes.
The echolocation calls of other bats have lower duty cycles Work on echolocation (e.g., Simmons and Stein 1980;
(<20%) and various combinations of broadband and narrow- Nachtigall and Moore 1988) and flight dynamics (e.g., Norberg
band FM components. Species foraging in open situations and Rayner 1987) generally supports the above view of bats'
usually produce narrowband search-phase echolocation calls access to different habitats. Aldridge and Rautenbach (1987)
 TABLE2. Comparison of some details of the foraging behaviour of various animal-eating bats, derived from observations of
known individuals canying radio transmitters

Longest One-way
flighta distanceb Foraging Same
n (min) (km) strategyc aread Source

Megaderma lyra CF, SF Yes Audet et al. 1988

Nycteris grandis CF, SF Yes Fenton et al. 1987
Nycteris grandis (from
same study site) CF, SF Yes Fenton et al. 1989
Rhinolophus hildebrandti CF, SF Yes Fenton and Rautenbach 1986
Myotis myotis CF Yes Audet 1990
Eptesicus fuscus
Ontario CF No Brigham and Fenton 1986
British Columbia CF Yes Brigham 1988
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Scotophilus borbonicus
Zimbabwe CF No Barclay 1985
South Africa CF No Fenton and Rautenbach 1986
Nyctalus noctula CF Yes Kronwitter 1988
Lasiurus cinereus
Manitoba CF No Barclay 1989
Ontario CF Yes Hickey and Fenton 1990
Lasiurus borealis CF Yes Hickey 1988
Euderma maculatum CF Yes Wai-Ping and Fenton 1989
Tadarida midas CF No Fenton and Rautenbach 1986
NOTE:n, sample size (number of bats), with number of bat days with one bat with an active radio for a 24-h period (= 1 bat day) in parentheses.
"Longest continuous flight recorded (min).
bDistance (km) between roost and foraging location.
CF, continuous flight; SF, short flights from perches.
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dIndicates whether individuals returned to the same foraging area every night.

examined several sympatric species in a southern African costs to the animals. Adults in some species alternate between
community and found a strong positive correlation between these two foraging strategies (Table 3), and in others the use of
echolocation call design and wing morphology relating to continuous flight versus flights from perches changes with age,
habitat use, as did Barclay (1988). Fenton and Rautenbach for instance, light-tagged young Myotis luczfugus foraged from
(1986) tested predictions about access to cluttered habitats by perches whereas light-tagged adults foraged from continuous
observing radio-tagged individuals. They found that the broad- flight (Buchler 1980).
winged Rhinolophus hildebrandti, with an echolocation system Switching between the two strategies appears to involve
specialized for flutter detection, foraged in thick riverine forest, broad-winged species that usually forage in closed and edge
whereas the narrow-winged Tadarida midas, which uses situations (e.g., Rhinolophus hildebrandti (Fenton and Rauten-
narrowband echolocation calls, foraged only in open habitats. bach 1986); Rhinolophus rouxi (Neuweiler et al. 1987)). Data
Scotophilus borbonicus, a species with wings of intermediate from species with long narrow wings (high aspect ratio) suggest
aspect ratio and wing loading and broadband echolocation calls, that they forage only from continuous flight, whether in edge or
operated from the edges of tree canopies out into more open, in open habitats (Table 2). In Nycteris grandis, a broad-winged
uncluttered areas. Crome and Richards ( 1988) used population species, allocation of time between the two foraging strategies
data to identify similar patterns of habitat use by some appears to reflect prey availability; when prey were scarce there
Australian bats. was a significant effect of habitat on the strategy adopted, and
The available data from flight dynamics and echolocation call significant variation between individuals (Fenton et al. 1989).
design permit workers to describe these features quantitatively Relative to times of abundant prey, these bats relied signifi-
and to make predictions about performance and access to cantly more on hunting from continuous flight than on hunting
different habitats by bats searching for prey. These predictions from perches (Fenton et al. 1989).
can be tested by challenging bats' manoeuvrability in obstacle Among species foraging from continuous flight there are two
courses (Aldridge and Rautenbach 1987) and by using active different search patterns with different search costs. There are
tags such as lights or radio transmitters to assess habitat use by species in which single continuous flights usually last less than
bats under natural conditions. 120 min , whereas others spend >300 min nightly in continuous
flight (Table 2). Switching between these two strategies seems
Functional Components to occur in one direction only, the long-duration fliers occasion-
By search cost (C,) ally making shorter flights. This situation may reflect the
Tabulation of data on the foraging behaviour of known physiology and structure of the flight muscles and associated
individuals (Table 2) suggests that animal-eating bats adopt one energy delivery systems.
of two basic strategies when searching for prey, namely
operating from continuous flight or from a perch (Fig. 4). As By prey selection (A and Ch)
Thomas (1987) has pointed out that flight in bats can increase The prey taken by a foraging bat will reflect the habitat in
energy consumption by 25 times over basal metabolic rate, which the animal is hunting and its ability to detect, locate, and
these two approaches represent dramatically different search handle the prey. The fundamental distinction between airborne
 CAN. J. ZOOL. VOL. 68, 1990

CONTINUOUS FLIGHT FLIGHTS FROM A PERCH

long flights T b short flights

(>300 min) (ca. 120 min)

AIRBORNE PREY NONAIRBORNE PREY

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SMALL PREY LARGE PREY

(<5% of bat's mass) (> 10% of bat's mass)
FIG. 4. The consequences of foraging strategy for prey selection (airborne versus nonairborne) and prey size; arrows identify possibilities
associated with different patterns of behaviour.

and nonairborne prey has consequences for the size of prey the ground to pursue prey. In Nycteris grandis (Fenton et al.
available to a hunting bat (Fig. 4). Airborne prey are usually 1989) and Megaderma lyra (Audet et al. 1988), nonairborne
flying insects, ballooning spiders, or other animals small prey are located from continuous flight or from perches. The
For personal use only.

enough to be blown aloft by wind. Nonairborne prey can include ability to use prey-generated cues when searching, as well as to
a wealth of small animals, such as insects, that can fly, as well as manoeuvre and achieve good lift, should characterize bats
larger prey items such as small terrestrial vertebrates and aquatic adopting this pattern of foraging. Furthermore, because attacks
organisms active at the water surface. may involve touchdowns and other expensive manoeuvres close
Bats foraging from continuous flight appear to rely mainly on to clutter, the costs of taking nonairborne prey may exceed those
airborne prey, limited to small prey items which require short of taking airborne targets. Animal-eating bats taking nonair-
handling times. For small bats, head, jaw, and tooth morpho- borne prey should resolve this situation by taking the largest
logy limit access to larger prey, and for many species foraging in available prey.
the open, wing morphology, specifically the ability to generate Species taking nonairborne prey have access to larger prey
lift, will constrain them in dealing with larger prey. Evidence items which require longer handling times. Bats that hunt from
from morphological studies of the teeth and jaws of animal- perches have significantly longer heads and tooth rows than
eating bats (Freeman 1979,1981) suggests that some species are those foraging from continuous flight, which may influence
better equipped than others to deal with hard insects such as their ability to deal with larger prey (Fenton 1989). As usual in
beetles. Bats foraging from continuous flight must encounter predator-prey interactions, larger predators have access to
prey at relatively high rates (A), and in the course of their larger and smaller prey, whereas smaller predators are limited to
feeding periods, successfully attack many individual items. smaller prey (e.g ., Aldridge and Rautenbach 1987).
Although encounter rates are not synonymous with attack rates, Echolocation call design could influence the size range of
the latter provide an impression of the incidence of prey that bats prey taken by some bats. Barclay (1986, 1988) suggested that
find appropriate. Published data on attack rates for species the relatively low frequencies of its echolocation call could
foraging from continuous flight range from 20 to 0.75lmin explain the failure of Lasiurus cinereus to include small insects
(Brigham 1988; Barclay 1986; Hickey and Fenton 1990; Wai- in its diet. The small insects would be undetectable by the bat
Ping and Fenton 1989), and success rates are around 40% because of the long wavelengths of the sounds in its calls.
(Vaughan 1977; Bell and Fenton 1984; Hickey and Fenton Schnitzler (1987) proposed that echolating bats might extend
1990). As many animal-eating bats consume 30-50% of their their range of detection by using narrowband calls whose
body mass nightly (e. g ., Anthony and Kunz 1977), it is possible duration exceeded the wingbeat cycles of their insect prey. This
to generate specific predictions about the incidence of attacks on would be achieved through the "glints" generated by differences
the basis of information about prey size. When other factors in reflective area over the insect's wingbeat cycle. In this sense,
are equal, species with longer interattack intervals should take the detection of glints is not analogous to the flutter detection
larger prey than similar-sized species with shorter interattack (via Doppler shift) of some other bats (see earlier).
intervals. Selection by size is a recurring result of studies comparing
Like some species of birds, some bats forage from continuous prey available to and prey taken by bats using echolation to find
flight and take nonairborne prey. Radio-tracking studies have airborne targets (e.g., Buchler 1976; Anthony and Kunz 1977;
identified Myotis myotis as one example (Audet 1990); it takes Bell and Fenton 1984; Belwood and Fullard 1984; Racey and
such prey as flightless carabid beetles (Bauerova 1978). The Swift 1985; Brigham 1988; Hickey and Fenton 1990). The
radio-tracking data shows no indication that M . myotis hunts mechanism for this pattern of prey selection may be range-tuned
from perches or makes more than brief (<30 s) touchdowns on neurons in the auditory cortices of echolocating bats (both
 TABLE
3. Predictions about the foraging behaviour of animal-eating bats generated by this review

FROM
HABITAT USE

1. Bats searching for prey in closed habitats will fly at lower speeds than those foraging in more open areas. Flight
speeds of species foraging in edge habitats will not differ significantly from those operating in open ones.
2. Bats with high aspect ratio wings and pointed wing tips that orient by narrowband echolocation calls will not forage
in closed or edge habitats.
3. Bats with low aspect ratio wings, low wing loadings, and rounded wing tips that orient by short, broadband echo-
location calls will search for prey in open, edge, and closed habitats.
4. The bimodal distribution of wing characteristics (aspect ratio, wing loading, and wing-tip shape) reported in the
Rhinolophidae and Hipposideridae (Norberg and Rayner 1987) suggests that within these families some species make
more use of closed habitats than others.
FROM
FORAGING STRATEGY ( C , )

5. Comparisons of similar-sized species foraging in open habitats will show that those with higher aspect ratios will
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consume less energy per unit flight time than those with lower aspect ratios, although this situation will be influenced
by wing loading.
6. Among species foraging from continuous flight there will be significant differences in muscle physiology and energy
delivery systems between those flying for long (>300 min) versus short (<I20 min) times.

7. Species foraging in closed habitats and taking mainly nonairborne prey will rely on prey-generated cues or on vision
to locate their targets.
8. Species in the Rhinolophidae and Hipposideridae and Pteronotus parnellii will feed mainly on flying insects or those
vibrating their wings, reflecting their echolocation systems which are specialized for flutter detection.
9. The auditory cortices of echolocating bats that hunt at long range will have more neurons tuned to longer time delays
than will those of species operating at short range.

10. Individual airborne prey items will be less than 5% of the bat's body mass, reflecting mechanical limitations
For personal use only.

associated with size.

11. The handling costs for airborne prey will be negligible and feeding rates will be limited by the rates at which prey are
encountered (A), not by handling time.
12. The handling costs for larger nonairborne prey will be significant and will affect feeding rates.
13. Echolocating bats selecting narrow ranges of prey size will have smaller search zones (defined by time and encoded
as time-delay neurons) than those taking wider ranges of prey size.
14. Longer feeding buzzes will represent greater investment in individual prey and correlate positively with larger
individual prey items.
15. Animal-eating bats will take specific prey taxa when feeding in monispecific clumps of prey, or when they rely on
prey-specific signals to find their targets (e.g., sexual advertising signals).

16. Variability in the behaviour of individuals will mean that the labels "gleaner," "piscivore," "carnivore," and "perch
hunter" will not fully describe the behaviour and foraging ecology of bats.

17. Behaviour and ecological data will reflect morphometric studies and show extensive overlap in foraging behaviour
and prey selection among sympatric animal-eating bats.

flutter detectors and other echolocators (O'Neill 1987)). These and short interpulse intervals, and the latter use longer echoloca-
neurons measure delay times (i.e., distance to target), and by tion calls of narrow bandwidth and longer interpulse intervals.
searching a specific range window, bats could increase the Furthermore, Balcombe and Fenton (1988) pointed out that
precision of selection by prey size by distinguishing between feeding buzzes (the high pulse-repetition rates associated with
closer, smaller targets from more distant larger ones. attacks on airborne prey (Griffin et al. 1960)) are longer in
The populations of time-delay neurons in the auditory Lasiurus borealis, a "long-range bat," than they are in the
cortices of echolocating bats should differ between species short-range Myotis lucifugus. Balcombe and Fenton (1988)
detecting and reacting to airborne targets at short or at long proposed that this represented greater investment in the pursuit
range (e.g., Brosset 1966; Fenton 1982; Barclay 1986). The of individual prey items. If true, this leads to the hypothesis that
behavioural distinction is based on direct observations of in similar-sized species, larger prey will be selected by bats
behaviour (e.g., Fenton and Bell 1979; Barclay 1986), differ- producing the longest feeding buzzes. At present there are not
ences in design of echolocation calls (Barclay 1986), and the enough data on feeding buzz durations and prey taken to
rates at which search-phase echolocation calls are produced challenge this hypothesis.
(Table 1). At a rich patch of prey (e.g., insects around a There is conflicting evidence about whether animal-eating
streetlight) short-range bats make several attacks per pass bats specialize on particular taxa of prey. Some analyses of fecal
through the patch whereas long-range ones make single attacks. or stomach contents indicate that bats may take a narrow range
The former use shorter echolocation calls of broader bandwidth of prey, but others suggest more diverse diets. Specialization
 418 CAN. J. ZOOL. VOL. 68, 1990

may be at the ordinal level (e.g., moths (Black 1974))or even at animal-eating bats, because of intraspecific variation in behav-
the species level (e. g .,one species of frog (Fenton et al. 1987)). iour and in prey consumed.
Where the data on prey taken are not accompanied by The proposal that big-eared bats are gleaners is widely
information about prey available to the foraging animals, they accepted. At some point, biologists studying bats identified
do not challenge the hypothesis about specialization. Schnitzler species that glean (take prey from surfaces) as representative of
(1987) reported that some flutter-detecting bats can distinguish a different strategem and proposed that species with large ears
between the wingbeat signatures of different species of insects, were gleaners. As large ears might add resistance during flight,
but it remains to be seen if they can exploit this ability when and because some large-eared, broad-winged bats were very
foraging in heterogeneous assemblages of prey. In many cases, manoeuvrable in flight, the proposal seemed logical. It became
a narrow range of prey consumed reflects only availability to more attractive when students of echolocation pointed out that
bats, e.g., to those foraging in homogeneous swarms of prey the perceptual problem facing gleaners (a hard target on a hard
such as hatches of emergent insects (for example, see Buchler surface) differed dramatically from the one confronting bats
1976; Brigham 1988). hunting airborne prey (a hard target on a soft background), and
Tuttle and Ryan (1981) demonstrated that Trachops cir- soon both the notion of gleaning as a separate strategy and the
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rhosus relies on the calls of male frogs to identify and locate association between big ears and gleaning were entrenched
them. In this case, the mode of prey detection allows the (e.g., McNab 1971; Humphrey et al. 1983; Hill and Smith
predator to be very specific in its selection by taxon, and the 1984).
same situation applies to bats exploiting the calling songs of Usually, this view of gleaning was based on the bats' diet
insects (Tuttle et al. 1985). Of course, the use of generalized rather than on their foraging behaviour. Vaughan (1976)
prey-generated cues (e.g., those associated with movement) to reported that Cardioderma cor, an African bat with large ears,
locate targets also can lead to a generalized diet (Ryan and Tuttle alternated between gleaning and pursuing airborne prey. Stud-
1987; Fenton et al. 1983; Bell 1982). Whether the bats are using ies on other species echoed Vaughan's (1976) findings, demon-
echolocation to find their prey or are relying on prey-generated strating that the small-eared Hipposideros cafSer (Bell and
cues, specialization may reflect prey availability as it does in Fenton 1984) alternated between taking prey from surfaces and
other predator-prey systems. from the air, as did Megaderma spasma (Tyrrell 1988), Myotis
It is tempting to predict that bats will exploit rich patches of emarginatus (Krull et al. 1988), and Myotis evotis (Faure
prey (high rates of encounter) to minimize foraging time. 1988). Variability in foraging behaviour suggested that glean-
ing species also pursued airborne targets. Furthermore, the bat
For personal use only.

Although many species of bats do so (e.g., Fenton and Morris

1976; Vaughan 1980; Gould 1978; Bell 1980; Furlonger et al. with proportionally the largest ears (Euderma maculatum)
1987; Brigham 1988), others do not. Wai-Ping and Fenton pursued airborne targets and showed no evidence of gleaning
(1989) found that foraging Euderma maculatum never visited (Leonard and Fenton 1983; Wai-Ping and Fenton 1989),
known (to them) artificial or natural patches of high insect challenging the traditional association between ear size and
density. At rich patches of prey, foraging bats should exhibit the gleaning behaviour.
greatest selectivity by size and (or) taxon to maximize their rates Gleaning involves taking nonairborne prey and it may be used
of energy return. in closed or edge habitats by bats foraging from continuous
flight or from perches. To have access to nonairborne prey a bat
Flexibility and decisions must be able to use prey-generated cues for locating its targets
The foregoing emphasizes the importance of flexibility in the and to fly slowly (low wing loading) in areas of high clutter
foraging behaviour of bats while identifying examples of some (requiring short wings). Although this set of features can be
species that have greater potential for flexibility than others. used to identify bats showing the potential to use nonairborne
Efficient use of energy-reflecting parameters such as search cost prey, all the species with these attributes for which we have data
(C,), prey encounter rate (A), and the cost of handling prey (Ch) also exploit airborne targets. The available data do not identify
imposes some limitations on flexibility, depending upon prey any animal-eating bats that feed only on nonairborne prey.
availability. This situation is reminiscent of Dill's (1983, 1987) Similarly, data on variability in foraging behaviour and diet
reviews of flexibility and decision making and their importance suggest that perch hunting, carnivory, and piscivory are
in the ecology of aquatic systems. For animal-eating bats, variations on a theme rather than distinctive strategies among
mechanical and perceptual features set functional limits which animal-eating bats. Species known to hunt from perches also
have repercussions for both habitat use and prey taken. In its forage from continuous flight (Table 2). The bats known to
broadest sense this means that sympatric animal-eating bats of include small terrestrial vertebrates in their diet also feed on a
the same size will behave the same, regardless of wing variety of invertebrates (Norberg and Fenton 1988), making it
morphology. And yet, flight dynamics resulting from wing inappropriate to label some species "carnivorous." As the
morphology will affect efficiency, so that species with high species identified as piscivores take aquatic organisms other
aspect ratio wings will always have more efficient flight in open than fish, and in some cases, flying prey (J. J. Wenstrup,
settings than species with lower aspect ratio wings. This means personal communication), this category is also inappropriate for
that C, will be an important variable in the equation, and the bats. Norberg and Rayner (1987) used "trawling" to identify
model of Mittelbach (1981) identifies the importance of C, and species that take prey from the surface of water, but most also
Ch in limiting an animal's options. take airborne prey. As these bats may forage from continuous
flight or by short flights, and because they forage in edge or
Gleaning, perch hunting, carnivory, and piscivory closed situations, taking prey appropriate to their size, there
It often has been proposed that among bats, gleaning, perch seems little justification for identifying carnivory or piscivory as
hunting, carnivory, and piscivory represent separate foraging separate strategies. Furthermore, the use of continuous flight by
strategies. This view is not supported by the preceding structural species that sometimes hunt from perches precludes regarding
and functional consideration of the foraging behaviour of perch hunting as a separate strategy. Bats in these categories use
 edge or closed situations, exploiting airborne and nonairborne periods (<120 min, E. fuscus). It is tempting to suggest that the
prey according to prevailing conditions. low frequencies in the echolocation calls of Euderma preclude
its locating smaller prey, but there are insufficient data on the
Bat communities diet of this species to challenge this hypothesis.
Morphometric analyses suggest that the species composing The foraging behaviour and pattern of habitat use of the
bat communities are closely packed, with a few dramatic sympatric Nycteris spp. and of E . maculatum and E. fuscus
outliers (Findley and Wilson 1982; Schum 1984). Even when illustrate the need to use behavioural data to categorize the
features such as echolocation behaviour and flight performance foraging of animal-eating bats.
are considered (e.g., Aldridge and Rautenbach 1987), general In November 1987, the bat fauna at the study site in Mana
similarity and a size gradient are prevailing features of commu- Pools National Park was dominated by species that hunt from
nities of animal-eating bats. This suggests that sympatric continuous flight (911 1 species, Fenton et al. 1989). This
species of bats are characterized by variations on themes situation, and the use of continuous flight by Nycteris spp.,
governing access to cluttered environments (wing morphology suggest that at low prey densities continuous flight is more
and echolocation call design) and affecting the ability to deal efficient than short flights from perches. In typical wet seasons
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with differences in prey size or hardness (tooth and jaw at other locations in Zimbabwe, species presumed to hunt from
morphology). Sympatric species should therefore show consid- perches are more common (31.5% of 19 species), suggesting
erable overlap in their use of foraging space and food resources. that foraging from continuous flight may be the only strategy
Data from times during which food shortages place bats under represented in habitats and situations that are marginal because
stress may offer an indication of the importance of variability in of prey availability. Temperate species of the Rhinolophidae
foraging behaviour. In November 1987 in Mana Pools National and Vespertilionidae may circumvent cold, inclement periods
Park in Zimbabwe, a drought coupled with high daytime by the use of torpor (Audet and Fenton 1988).
temperatures coincided with a shortage of airborne and nonair-
borne prey for 35-g Nycteris grandis (Fenton et al. 1989) and Conclusion
10-g Nycteris thebaica (Aldridge et al. 1990). Data from This treatment of the data on the behaviour and ecology of
individuals carrying active tags (radio transmitters for N . foraging bats generates a number of predictions testable with
grandis and light tags for N . thebaica) revealed that both species bats in the laboratory and field (Table 3). The access of
alternated between foraging from continuous flight and flights animal-eating bats to prey in habitats with differing levels of
from perches. The data also showed that the bats flew in habitats clutter (closed, edge, open) is determined by mechanical
For personal use only.

ranging from wide open spaces within 0.5 m of the ground or features associated with wing morphology and by sensory
water to areas in closed habitats. Their pattern of use of hunting features associated with echolocation call design and the ability
perches varied according to the availability of these, but even in of bats to use prey-generated or visual cues to find their targets.
edge settings with perches available, the bats often hunted from Animal-eating bats may forage from continuous flight or by
continuous flight. In November and early December 1987, making short flights from perches, and may take airborne or
individual N . grandis took <4 g of food per night, compared nonairborne prey. Species taking nonairborne prey have access
with ca. 10 g of food in early December 1985, when there had to large prey (>lo% of the bat's body mass), whereas those
been rains in November; these data indicate stress associated hunting airborne targets are restricted to smaller prey (<5% of
with prey availability. Both species have low aspect ratios, low body mass). Among species foraging from continuous flight,
wing loading, and rounded wing tips, and use short, low- some fly for extended periods (>300 midnight), whereas
intensity, high-frequency broadband echolocation calls while others make shorter flights (<120 midnight).
relying upon prey-generated cues to find targets (Fenton et al. Flexibility produces individual variability which confounds
1983). This provides an example of the flexibility leading to clear-cut categorizations of foraging bats. Mechanical and
structural and functional switching identified earlier. perceptual constraints, however, dictate that most of the
Another indication of the difficulty of using morphological or flexibility works in one direction. This means that species
echolocation call parameters to identify the foraging behaviour adapted to operate in closed habitats have access to edge and
of bats is provided by the comparison of sympatric Eptesicus open habitats, but those adapted for open settings have very
fiscus and Euderma maculatum (Brigham 1988). There are no limited access to closed and edge habitats. In this example, the
significant differences between these species in body mass limiting factors are the mechanical and sensory ability to deal
(18.6 + 2.7 (SD) vs. 17.9 + 2.1 g), wing loading (1 1.9 + 1.6 with clutter. Species that sometimes hunt from perches also
*
vs. 10.3 1.1 N-m-*),aspectratio(7.0+ 0 . 6 ~ s7.0 . +0.4), forage from continuous flight, and there is no evidence of the
or wingspan (0.33 1 + 0.12 vs. 0.346 + 0.07 m). Both species reverse trend in adult bats. Species taking nonairborne prey
forage from continuous flight, but E. maculatum consistently probably detect them by means of prey-generated cues, and may
flies for much longer than E. fuscus (Table 3). Both species feed also include airborne prey in their diet. Species relying on
on airborne prey and use short (4-6 ms) broadband echolocation airborne prey appear to use echolocation, and their inability to
calls. Euderma maculatum has huge ears and uses echolocation use prey-generated cues may deny them access to nonairborne
calls of much lower frequency than those of E. fuscus (most targets. Large bats can take small prey, but morphological
power at 10 vs. 30 kHz (Brigham 1988)). In spite of the constraints preclude the converse.
similarity in wing morphology, E. maculatum has lower Communities of animal-eating bats are composed mainly of
relative wing loading (39.3) than E. fuscus (44.9), so it should similar species, suggesting considerable overlap in patterns of
be able to fly more slowly and somewhat less expensively resource use. Foraging from continuous flight, probably in edge
(U.M. Norberg, personal communication). Apart from relative situations, is a widespread strategy among animal-eating bats
wing loading there are no overt morphological or echolocation which appears to be very resistant to situations of low prey
features distinguishing the species that flies for long periods availability. Wing morphology may contribute to this because
(>300 min, E. maculatum) from the one that flies for shorter of the low costs of flight.
 420 CAN. J. ZOOL. VOL. 68, 1990

Acknowledgements
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