BlOTROPlCA 33(4): 670-681 2001

Dietary Benefits of Twilight Foraging by the Insectivorous Bat Hipposideros speoris’

Chris I?. Pavey2

Zoology Institute, University of Munich, Luisenstrasse 14, Munich 80333, Germany

Chris J. Burwell

Queensland Museum, P.O. Box 3300, South Brisbane, 4101, Queensland, Australia

Jan-Eric Grunwald

Zoology Institute, University of Munich, Luisenstrasse 14, Munich 80333, Germany

Chris J. Marshall

Queensland Department of Natural Resources, 1345 lpswich Rd., Rocklea, 41 06, Queensland, Australia

and

Gerhard Neuweiler

Zoology Institute, University of Munich, Luisenstrasse 14, Munich 80333, Germany

ABSTRACT Although bats are nocturnal, many species emerge from roosts to forage during twilight, despite a presumed high risk of predation at this time. Here, we describe twilight foraging by a maternity colony of Schneider’s leafnosed bat (Hipposideros speoris) in the dry zone of Sri Lanka and determine the dietary benefits of such behavior. Bats usually began foraging during dusk, sometimes before sunset, and also foraged during twilight in the morning. Mean use of available twilight by four radio-tagged bats was 75 percent. Twilight foraging made up, on average, 47 percent of the total foraging time of these bats (range = 25-96%), although twilight consisted of only 12 percent of the available time between sunset and sunrise the next morning. Eight species of potential predators (7 birds and 1 mammal) were observed within a 1 km radius of the colony, of which 5 species are predicted to regularly capture bats. Bats took a wide diversity of prey (1 1 insect orders, including at least 27 families, and spiders) that ranged in wing length from 2.0 to 54.0 mm. Major orders in the diet were Coleoptera, Lepidoptera, and Diptera. Prey of secondary importance included Hemiptera, Hymenoptera, Isoptera, and Neuroptera. Bats captured large numbers of insects that were only available or had marked peaks in abundance during twilight. These groups included small, swarming insects (especially flies) that have peaks in flight activity at dusk and dawn, large diurnal species (especially dragonflies) that have crepuscular activity, and winged termites that emerge in swarms at dusk. Access to these insects was a clear benefit of twilight foraging.

Ki word: activity patterns; bats; diet; foraging; Hipposideros speoris; nautical twilight; predation; Sigirzja; Sri Lanka.

BATS (CHIROPTERA) ARE A DIVERSE A N D WIDELY DIS-

TRIBUTED ORDER of mammals that forage almost ex- clusively during night (ie., between sunset and sunrise; Speakman 1990, 1995; cf: Thomson et al. 1998). Although the risk of predation faced by bats is presumed to be greater during twilight ( i e . , dusk and dawn) than true night, many species leave their roosts before dark (Jones & Rydell 1994), poten- tially exposing themselves to diurnal predators (Fenton et al. 1994). Twilight activity must have

’ Received 16 May 2000; revision accepted 18 December 2000.

Current address and address for correspondence: Parks and Wildlife Commission of the Northern Territory, Arid Zone Research Institute, PO. Box 1046, Alice Springs, Northern Territory, Australia 0871.

considerable fitness benefits for the behavior to per- sist in the face of high predation risks (Duvergk et al. 2000).

Jones and Rydell (1994) have proposed that twilight activity allowed bats to exploit Nematocera and other small flies that show marked peaks in flight activity during twilight (especially at dusk) and very little activity during most of true night (Pandian & Chandrashekaran 1980, Racey & Swift 1985, Rydell et al. 1996). Twilight foraging by bats, however, has other potential benefits, espe- cially in tropical regions where insect diversity is very high. First, bats can gain access to groups of insects (particularly winged termites and ants) that emerge in large numbers at dusk. Further, bats can increase their prey range by capturing diurnal in- sects during twilight (Pavey & Burwell 1998).

670

Twilight Foraging by Bats 671

Many of these insects are large in size, and there- fore represent profitable prey. Last, bats can in- crease the available foraging time by being active at dusk and dawn. The length of twilight varies with latitude, but even in the tropics where its du- ration is the shortest, twilight activity can increase foraging time by up to 90 minutes. An increase in available foraging time may be very important for female bats during pregnancy and lactation, a pe- riod when nutrient and energy requirements are high (Barclay 1995).

In this study, we describe the timing of foraging activity in Schneider's leafnosed bat (Hipposideros speoris), a tropical species that uses constant fre- quency (CF) echolocation calls for orientation and prey detection (Habersetzer et al. 1984, Jones et al. 1994). Hipposideros speoris is a medium-sized (mass = 9.0-14.5 g; forearm length = 45.6-54.0 rnrn), insectivorous bat that is common in Sri Lanka and India (Bates & Harrison 1997). We studied bats at a maternity colony in Sri Lanka, where preliminary observations indicated that twilight foraging was common. Therefore, we assessed the potential di- etary benefits of such behavior. The main aims of the research were to: (1) determine both the du- ration of available twilight that was used for for- aging and the proportion of foraging that took place during twilight; and (2) assess levels of pre- dation on insect groups that were only available or reached their peak abundance during twilight. In addition, we recorded potential predators active in the vicinity of H. speoris roosts and foraging areas during twilight to gain an impression of the pre- dation risk faced by twilight-active bats.

METHODS STUDY sirE.-we carried out the study from 16 March to 30 April 1999, at a maternity colony of ca 1 100 adult H. speoris containing both sexes. Bats roosted in two small caves, within 100 m of each other, at the base of Sigiriya Rock in central Sri Lanka (07"57'N, 80'46'E). The caves are located within the Ancient City of Sigiriya, a World Her- itage Site proclaimed in 1982. Sigiriya Rock is a granite peak rising 200 m above the surrounding plain (377 m elev.). A 40 ha area of parkland and ornamental gardens is located immediately to the west of Sigiriya Rock. The remainder of the site consists of a mosaic of land uses. Most land within a 2 km radius of the bat roosts is a wildlife sanc- tuary within which the vegetation is dominated by closed forest; however, large portions of land close to Sigiriya Rock consist of human settlement, ag-

ricultural fields, and reservoirs (see Pavey et a/. 2001 for a map and further details).

Most adult females in the colony were pregnant at the start of the study. Parturition began on 25 March and continued until the end of the study, with a peak in births between early and mid-April. A count on 18 April recorded 530 young in the two roosts. We did not observe other bat species roosting in the caves.

FORAGING Ac-riviru.-we obtained data on time of commencement and completion of foraging and on the duration of foraging by observing the activ- ity of radio-tagged individuals. We caught eight adult H. speoris (five males and three lactating fe- males) with a hand net at the roost entrance and glued a 0.5 g radio transmitter (model LB-2, Ho- lohil Systems, Carp, Ontario, Canada) on the dor- sal surface between the shoulders of each animal. Transmitter mass was less than 5 percent body mass (mean transmitter mass = 4.1 2 0.2% of body mass; range = 3.@.7%). Tagged bats were re- leased back into the roost within one hour of cap- ture. We began to track each bat on the night after a transmitter was attached. We used Regal 2000 (Titley Electronics, Ballina, NSW, Australia) and Merlin- 12 (Custom Electronics, Urbana, Illinois) receivers with 5-element Yagi and H frame anten- nae.

Usually, two bats had transmitters attached at any time; however, on most nights we tracked only one bat. We attempted to track the target bat con- tinuously throughout the night from the time it left the day roost until the end of the final foraging bout the next morning. We used a combination of a stationary and mobile tracking unit. The station- ary tracking unit was positioned on the northwest- ern slope of Sigiriya Rock, very close to the en- trance of the two roosts. A single observer ran it. The mobile tracking unit involved two observers following the target bat either on foot or (rarely) in a vehicle. Observers kept in contact using hand- held two-way radios. Because the mobile unit was often in closed forest, the range over which signals were detected was often low ( 2 1 0 0 m). The sta- tionary unit could detect signals at least 2 km away and up to an estimated 3 km.

Both units continuously monitored signals from the target bat once it left the roost. The mo- bile unit attempted to follow the bat to its foraging grounds. If the signal was lost as observers moved across the landscape, the bat was relocated with guidance from the stationary unit. In foraging ar- eas, the mobile unit determined a bat's location

672 Pavey, Burwell, Grunwald, Marshall, and Neuweiler

either by taking sequential directional locations from different sites (Barclay et al. 2000) or circling the area from which a signal was received on foot (Pavey 1998).

We recorded information on location and be- havior of tagged bats onto microcassette tape re- corders for subsequent transcription. Behavior dur- ing the night was classified as one of four types: ( 1 ) continuous flight. A bat foraged while flying over a small area and often made sudden changes in direction and/or height as indicated by sudden changes in signal intensity; (2) commuting flight. A bat flew rapidly and directly from one location to the next: (3) perching. A bat was stationary (pre- sumably perched in a tree) at a foraging site; and (4) night roosting. A bat was perched in a roost between bouts of flight.

In addition to the radio-tagging data, we re- corded the times when bats began foraging in five areas between 50 and 500 m from the roosts. The sites included all types of habitat occupied by for- aging H. speoris and the amount of canopy cover present ranged from 100 to 0 percent. Observers waited at the sites prior to sunset and recorded the time when the first H. speoris began foraging.

We defined dusk as the period between sunset and the end of nautical twilight (defined as the instant when the center of the sun is 12" below the horizon) and dawn as the period between on- set of nautical twilight and sunrise. We chose nau- tical twilight rather than the more commonly used civil twilight because the former clearly demar- cates solar light from true night (star and lunar light; Brigham & Barclay 1992). The duration of twilight each night during the study period was 90-94 minutes (45-47 min at dusk and dawn). We obtained data on local sunset and sunrise times and length and times of nautical twilight from the database of the Australian Surveying and Land Information Group (AUSLIG), Common- wealth of Australia.

SURVEY OF POTENTIAL PREDATORS.-DUTing the study period, we surveyed potential bat predators within a 1 km radius of roosts, although most search effort was within an area of 20 ha around the roosts. Diurnal birds were counted and iden- tified in all habitats by walking along tracks and roads and across open fields. Within closed forest, intensive searches were also carried out away from tracks and roads. Nocturnal vertebrates were sur- veyed by driving and walking the network of tracks at night. In addition, many records were obtained

via incidental observations during the course of other activities.

To determine if predators were active around the roosts at dusk, one observer (CRP) spent ca 60 minutes (30 min prior to and following sunset) on each of five nights searching the 20 ha around the roosts. In addition, observers noted all potential predators seen both near roosts and at foraging ar- eas of H. speoris. All potential predators were iden- tified using reference books (Phillips 1980, Harri- son & Worfolk 1999) and their numbers recorded.

Die-r.-we examined the diet of the study col- ony by identifying both animal fragments in fe- cal pellets and remains of prey dropped below feeding roosts. A sample of 75 to 100 feces was collected every seven to ten days from plastic sheets placed below roosts of H. speoris for at least 24 hours. We did not capture individual bats because of the high level of disturbance this action would have caused the maternity colony. We examined 50 feces from each of five dates (18 and 30 March; 9, 18, and 29 April) spread across the study period.

Feces were chosen at random from the sam- ple collected on each date. Each pellet was placed in a petri dish and four or five drops of 10 per- cent KOH were added directly to the pellet. The pellet was teased apart within two to three min- utes and covered in 70 percent ethanol. We sys- tematically searched each pellet for identifiable material under a low power (6.4-4OX) binocular microscope. Prey items were identified to the lowest taxonomic level possible. We recorded whether a taxon was present in each fecal pellet and the percent by volume of each order in each pellet was visually estimated to the nearest 5 per- cent. We estimated percent by volume only at the ordinal level because of the small amount of material that we could identify to family or ge- nus. We did not record Lepidoptera as present in a pellet if only traces of scales were identified. We counted all identifiable wing, leg, and head fragments of each taxon in each pellet and mea- sured the length (mm) of each intact wing.

We collected discarded remains of prey items of H. speoris from the floor of the day roosts and a night roost at least once weekly. We collected remains after bats departed the roosts at dusk (day roosts) or at dawn (night roost), by thor- oughly searching the floor of the roost with the aid of a headlight. All insect material that ap- peared to have been discarded by bats as they fed was collected. Subsequently, insects we observed

Twilight Foraging by Bats 673

living in the roosts (ie., Blattodea, Coleoptera: family Trogidae and subfamily Scarabaeinae) were excluded from our assessment of prey re- mains because they may not have been consumed by bats. All identifiable remains were classified to the lowest taxonomic level possible (by CJB) via reference to specimens in the collection of the Queensland Museum, Australia. We calculated the number of individuals of each family taken during each collection period on the basis of the numbers of body parts present. We measured the length (mm) of intact elytra (Coleoptera) and wings (all other taxa).

We classified each insect order and family ac- cording to whether it was more likely to be en- countered by foraging bats during twilight or true night. T h e twilight category included diur- nal species with crepuscular activity and noctur- nal species that show a marked peak in activity during dusk and dawn. Our classification was based on previous experience pertaining to the families in other tropical areas and observations of their activity patterns at Sigiriya. We accept that not all members of a particular ordedfamily have the same activity patterns; however, our aim was to classify each taxon on the basis of its most typical activity pattern.

STATISTICAL ANuysis.-Statistical analyses consisted of Mann-Whitney U-tests (Siege1 & Castellan 1988) performed using Statistica version 5.5 (Statsoft Inc., Tulsa, Oklahoma). We adopted an alpha value of 0.05. Data are presented as means 2 standard error.

RESULTS O V E R V I E W O F RADIO-TAGGING DATA.-we attempted to track radio-tagged bats on a total of 20 nights in March and April (Table 1). O n 13 nights, we were able to maintain radio contact for over 90 percent of the time (>98% on 11 nights) from the time a target bat departed its roost at dusk to that of its return from the final foraging bout at dawn the next morning. We disregarded all nights with less than 90 percent contact time, except for bat 4 on one night when we recorded the first and last foraging bout (Table 1); heavy rain prevented us from tracking it throughout the night.

Radio-tagged bats foraged only during contin- uous flight. We recorded bats perched at foraging sites for a combined total of 13 minutes. We as- sumed that these bats were either resting or feeding on prey, because we did not record any short

674 Pavey, Burwell, Grunwald, Marshall, and Neuweiler

flights. Such flights are characteristic of hipposi- derid species that forage by perch hunting (Vaughan 1977, Pavey 1998, Pavey & Burwell 2000). Commuting flights were generally very brief (< 1 min) as most bats began and finished foraging close to their roosts. We tracked bats up to 2 km from the day roost; however, on most occasions, tagged bats did not commute directly to these for- aging areas but instead foraged in intermediate lo- cations as they gradually moved away from the roost.

COMMFNCFMtN I AN11 C O N < 1 LlZlON Ot tORAC,lNL.-

Unmarked and tagged bats arrived at foraging areas just before or soon after sunset (Table 2). Un- marked bats commenced foraging at or before sun- set in two of five sites examined. Three of the tagged bats began foraging before sunset on at least one night (Table 2). We found no significant dif- ference in time of commencement of foraging be- tween unmarked and radio-tagged bats (Ul4, 14 = 98.0, P = 1.0). Tagged bats foraged during nau- tical twilight in the morning on all nights; however, bats finished foraging prior to sunrise on all nights of tracking (Table 2).

A<:Tlvl.m P A I T E R N S A N D PROPORTION OF TWILIGHT

FoRAclNc.-Mean nightly duration of foraging by radio-tagged bats was relatively short (161 2 13.7 min; range = 69-242 min; N = 13), whereas bats spent most of the night in roosts (mean duration of night roosting 513 2 14.6 min; range = 409- 617 min; N = 13). Tagged bats had two peaks of foraging activity; the first was between 1840 and 2030 h and the second between 0400 and 0630 h. A similar activity pattern was exhibited by the col- ony as a whole. Bats began congregating at night roosts from 2000 h onward and continued to oc- cupy these in large numbers until cu 0500 h. To illustrate this pattern, the number of bats occupy- ing a night roost over a two-hour period beginning at sunset on 12 April was: 1848 h (2 bats); 1910 h (20); 1940 h (35); 2010 h (140); and 2040 h (at least 250). Night roosts included the two day roosts, another cave close to the day roosts, and culverts under roads.

Radio-tagged individuals used most of the available twilight for foraging each night (mean use of twilight 74.7 2 3.5%; range = 5 4 9 6 % ; N = 14). Further, almost half of all foraging took place during twilight (47.0 t 5.3%; range = 25-96%; N = 13). This value varied between and within individuals (Fig. 1). For example, bat 3 spent 96 percent of its foraging time during twilight on the

0

x n

3 C 0 .- Y

3

cr

Twilight Foraging by Bats 675

300

250

- 200 -

E

6 100

'= 150 m - m

U

50

0

OTrue night .Twilight

3 3 4 7 7 7 7 7 7 i a a a

Bat number

FIGURE 1. Amount of time spent foraging during twi- light and true night by radio-tagged Hipposideros speoris at Sigiriya, Sri Lanka. Data are for nights when bats were in contact for at least 90 percent of the time between emergence at dusk and final reentry the following morn- ing.

first night of tracking, but only 28 percent on the fifth night. Although use of twilight for foraging was high, twilight made up on average only 12 percent (92.3 ? 0.3 min) of the mean time be- tween sunset and sunrise the following morning (792.5 ? 1.0 min) during the period of radio tracking at Sigiriya.

POTENTIAL PREDATORS AND EVIDENCE OF PREDA-

noN.-We recorded 115 species of birds (includ- ing 4 nocturnal species), 10 species of mammals (excluding bats), and 4 species of snakes within a 1 km radius of the roosts at Sigiriya. From this list, we considered 7 bird species and 1 mammal to be

potential predators of foraging and commuting bats (Table 3).

We did not observe any interactions between bats and their predators during the course of the study. Predators did not congregate at the entrances of H. speoris roosts at dusk or dawn ( N = 37 nights of observation) and we did not observe any pre- dation attempts in foraging areas or as bats com- muted from roosts to foraging areas. Neither did we observe any non-predatory birds harassing bats during twilight flight.

DiE-r.-We recorded 11 insect orders and spiders (Araneae) among fecal pellets and prey remains of H. speoris. All orders identified among prey remains were present in feces. At least 27 insect families were captured by H. speoris.

The importance of different insect orders in fe- ces of H. speoris varied according to the measure used to assess abundance. The three main orders in terms both of percent by occurrence and percent by volume were Coleoptera, Lepidoptera, and Dip- tera (Table 4). Hemiptera was the only other order with a percent by volume of more than 5. Diptera dominated feces in terms of the number of iden- tifiable fragments. The main family as measured by number of fragments was Culicidae (mosquitoes), which made up 15 percent of all identified frag- ments. Coleoptera, Neuroptera, Hymenoptera, He- miptera, and Isoptera all consisted of greater than 5 percent of identified fragments (Table 4). Cole- optera, Isoptera, and Lepidoptera were the most frequently recorded orders among prey remains (Table 5) .

TABLE 3. Potential predators of bats observed within a I km radius of H . speoris roosts at Sigirba, Sri Lanka.

Species (head and body length in mm) Activity patternsldistribution at Sigiriya

Birds Shikra Acc@iter badius (30-34)

Crested Serpent-eagle Spilornis cheela (61)

Changeable Hawk-eagle Spimetus cirrhatus (60)

Peregrine Falcon Falco p . peregrinator (38-44)

Indian Scops Owl Om bakkomoena (23)

Oriental Scops Owl 0. suniu (17)

Brown Fish Owl Bubo z. zeylonensis (54)

Mammals Common palm civet Paradoxurus hermaphoditus (47-56)

Diurnal and crepuscular; present at foraging

Diurnal; present at foraging areas but not ob-

Diurnal and crepuscular; active within 100 m of

Diurnal and crepuscular; active within 100 m of

Nocturnal, possibly crepuscular; active at forag-

Nocturnal and crepuscular: active at foraging

Nocturnal, crepuscular, and partly diurnal; active

areas.

served during twilight.

roosts until 1855 h.

roosts until 1900 h.

ing areas at night.

areas at night, dusk, and dawn.

around roosts from 1815 h onward.

Nocturnal; active around roosts and at foraging areas from ca 1915 h onward.

676 Pavey, Burwell, Grunwald, Marshall, and Neuweiler

TABLE 4. Percent by occurrence, percent by fiequenry (offiagments), and percent by volume ofprey items in fires (N = 250) of H . speoris fiom Sigiriya. Sri Lanka. Elurne data are presented only at the ordinal level. Orders or families dominated by species most likely to have been encountered by bats during twilight are marked in bold.

Percent No. of Percent Percent Prey taxon occurrence fragments fragments volume

Coleoptera 47.9 Curculionidae 1.6 9 0.9 Scaraboidea 3.2 8 0.8 unidentified 88.4 145 14.6

Lepidoprera 73.2 15 1.5 21.5 Diptera 16.3

Nematocera Culicidae 14.8 149 15.0 Chuonomidae 2.4 19 1.9 Mycetophilidae 0.4 1 0.1 Tipulidae 1.6 4 0.4 Unidentified 12.8 53 5.3

Brachycera Cyclorrhapha 16.8 134 13.5 Orthorrapha 0.4 1 0.1 Unidentified 2.4 12 1.2 unidentified 22.0 78 7.8

Hemiptera 5.1 Homoptera Fulgoroidea 0.4 2 0.2

Heteroptera 15.6 33 3.3

Formicidae 2.0 13 1.3 Ichneumonidae 0.4 2 0.2 Unidentified 20.8 76 7.6

Hemerobiidae 0.4 4 0.4 Unidentified 5.2 94 9.4

Unidentified 10.4 31 3.1

Hymenoptera 3.2

Neuroptera 1.1

Odonata 2.0 11 1.1 0.3 Psocoptera 2.0 7 0.7 0.2 Orthoptera 0.8 2 0.2 0.1 Isoptera 3.6 56 5.6 3.5 Blanodea 0.8 2 0.2 0.1 unidentified orthopteroid 6.0 27 2.7 2.1 Araneae 2.4 8 0.8 0.2 Total 996 99.9

Many of the insects we recorded in the diet of H. speoris were most likely captured during twi- light (Tables 4 and 5), including 31 of 83 (37%) individuals among prey remains. Twilight-active insects included typically diurnal groups such as Odonata (dragonflies) and Pieridae (butterflies), and families of small flies (Culicidae and Chiron- omidae) that have marked peaks of flight activity during twilight. In addition, bats captured ter- mites (and possibly ants) as they emerged in large numbers at dusk. We observed swarms of emerg- ing termites on 3 of 38 nights during the study period at Sigiriya. On one evening, we recorded a group of H. speoris feeding on an emerging swarm between 1850 and 1902 h. Although the first bat

was observed in the area only at 1844 h, 15-20 individuals were at the swarm and actively feeding by 1850 h. The swarm had disappeared before the end of twilight.

Size of prey captured by H. speoris, based on length of intact wings in feces and on the floor of roosts, ranged from 2.0 to 54.0 mm. The length of the majority of wings present in feces was less than 5.0 mm and none was greater than 25.0 mm (Fig. 2). The sample was composed mostly of dip- teran ( N = 36) and hymenopteran ( N = 13) wings. In contrast, most wingdelytra found among prey remains were greater than 15.0 mm in length and none was less than 5.0 mm (Fig. 2). The dif- ference in wing length between insects present in

Twilight Foraging by Bats 677

TABLE 5. Families of insects recorded among prey remains of H. speoris at Sigiriya, Sri Lanka. Orders or families dominated by species most like4 to have been encountered by bats during twilight are marked in boId. Size data are based on length of intact elytra (Coleoptera) or wings (all other taxa).

Mean size -t SE Order Order total Family Number (N)

Odonata 8 Aeshnidae 5 52.0 rf- 2.0 (2) - Libellulidae 1

Gomphidae 1 42.0 Unidentified 1

Orthoptera 4 Acrididae 1 19.5 -

- Tettigoniidae 1 - Unidentified 2

Coleoptera 32 Ceram bycidae 1 29.5 Buprestidae 1 8.5 Bostrychidae 1 13.0 Scarabaeidae 19 11.6 t 1.4 (6 )

Unidentified 8 7.8 rf- 1.3 (2) Noctuidae 3 16.0 ? 1.0 (3 ) Sphingidae 3 28.2 t 8.0 (3) Pieridae 1 19.5 unidentified 5 15.5 ( 1 ) Fulgoridae 1 14.0 Pentatomidae 1 Reduvidae 1 19.0 Ciadidae 1 28.0

Vespidae 2 9.0

Hydrophilidae 2 10.0 ( 1 )

-

Hymenoptera 7 Formicidae 5 14.5 ? 4.5 (2 )

Isoptera 14 14 22.1 rf- 0.4 (14) Neuroptera 2 Ascalapidae 2 36.5 rf- 6.5 (2) Total 83 83 21.4 t 1.7 (43)

Lepidoptera

Hemiptera

12

4

feces and prey remains was highly significant (4.1 +- 0.4 versus 21.4 5 1.7 mm; U,, 43 = 64.5, P < 0.001).

1 W Faeces 0 Prey remains

<5 5-10 10-15 15-20 20-25 >25

Size class of prey (wing length mm)

FIGURE 2. Frequency distribution of prey sizes in feces (N = 66) of Hipposideros zpeoris compared to that of prey remains below feeding roosts (N = 43).

DISCUSSION Our data on activity patterns of a maternity colony of H. speoris showed that bats foraged extensively during twilight. Bats began foraging around sunset and another peak in foraging activity occurred pri- or to sunrise. Twilight activity was noted both for a sample of radio-tagged bats and the colony as a whole. Not only was a high proportion of available twilight used for foraging, on average, 47 percent of total foraging time occurred during twilight. Al- though the sample of radio-tagged bats was small, patterns of commencement of foraging and night roosting of the entire colony appeared to closely match those of the tagged bats.

Patterns of emergence, reentry, and foraging ac- tivity of a colony of H. speoris a t Madurai (09"58'N, 78"10'E), south India (Marimuthu 1984), differed from those of our study colony. At Madurai, the first bat to depart a colony of ca 500 H. speoris left ca 10 to 20 minutes after sunset and

678 Pavey, Burwell, Grunwald, Marshall, and Neuweiler

the last bat to reenter arrived ca 10 to 25 minutes before sunrise (Marimuthu 1984). This pattern was observed over a period of 14 months covering the annual reproductive cycle. Activity levels of H. speo- ris at a foraging site 8 km from Marimuthu’s study colony showed three peaks of activity, all of which were during darkness: 2 100-2200, 2300-0 100, and 0200-0400 h (Habersetzer et al. 1784). The differences in twilight foraging and peaks of activity between the colonies at Madurai and Sigiriya, which were within 380 km of each other, support previous research that emergence and foraging be- havior of bats shows intraspecific variation in re- sponse to local conditions (Jones et al. 1775, Du- vergt et al. 2000). We suggest that bats in the Ma- durai colony emerged later because of an increased predation risk. In contrast to the Sigiriya colony, predators were present around the roost entrance at Madurai during dusk and owl predation oc- curred on at least one evening (Marimuthu 1984).

Although we did not observe any predation or attempted predation on H. speoris during the study, eight potential bat predators (four species of rap- tors, three owls, and one mammal) were active within a 1 km radius of roosts. Of this total, three raptor species (Spizaetus rirrbatus, Falro peregrinus, and Arcipiter badius) and two owls (Otus bakko- moena and 0. sunia) are known or predicted to prey on bats similar in size to H. speoris (Neuweiler et al. 1987, del Hoyo et al. 1994, Konig et al. 1999). All five species were likely to have been ac- tive at Sigiriya during twilight (Table 3).

The lack of observations of predators attack- ing H. speoris does not indicate that these bats do not face a potential predation risk during twilight activity. Rather, it is likely that the rarity of such interactions reflects a strong selection pressure on individuals that fly at the wrong time, either be- cause they make mistakes or take risks (Duvergt et al. 2000, Speakman & Rydell 2000). Also, it is possible that the flight behavior of H. speoris at Sigiriya lowers the risk of predation. Foraging in- dividuals flew close to surfaces-foliage, tree trunks, water, or the ground-irrespective of hab- itat. Height above surfaces was never more than 2 m and usually within 0.5 m. Further, bats flew relatively faster in more open habitats (e.g., park- land and pond), whereas flight was relatively slow in closed forest (Pavey et al. 2001). Such behavior is very likely to decrease the predation risk because raptors and owls face an increased risk of injury resulting from collisions while attempting to cap- ture prey close to surfaces (Newton et al. 1982).

Given that individual H. speoris at Sigiriya

could lower the risk of predation further by emerging during true night, they must obtain considerable benefits from twilight foraging for this behavior to persist. A potential benefit is that twilight activity allows bats to increase available foraging time, which may be important for fe- males during pregnancy and lactation when re- source requirements are high (Barclay 1995); however, this clearly was not the case during our study. Bats foraged for a relatively short time each night (mean for radio-tagged bats was 161 min out of 792 min of available time between sunset and sunrise the next morning), whereas most of the night was spent roosting. Radio-tagged indi- viduals concentrated foraging activity during twi- light, spending 47 percent of total foraging time during 12 percent of the time (from sunset to sunrise) taken up by twilight. This observation strongly suggests that bats selected the twilight pe- riod because it provided favorable foraging con- ditions.

Another explanation of twilight foraging is that it enables bats to gain access to insects that are either not present or not available in large numbers during true night. Our dietary data showed that H. speoris fed heavily on such insect groups during twilight activity. Bats captured both diurnal insects that are active at dusk and noctur- nal species that have marked peaks in activity at dusk and dawn. Based on both percent by occur- rence and number of fragments in feces, Diptera were the major prey of H. speoris during twilight activity. Mosquitoes (Culicidae) and other Ne- matocera were frequently captured, as were indi- viduals of the Cyclorrhapha. Our findings support an analysis of 66 bat species across 11 families, which showed that species that feed mainly on small, aerial prey, and therefore that are largely dependent on the dusk peak in flight activity of Diptera, tend to emerge earlier than other bats (Jones & Rydell 1994). Indeed, tropical bats feed- ing on small aerial insects were the only foraging guild with a mean emergence time prior to sunset (Jones & Rydell 1994).

Although many bats feed heavily on Diptera, most species do not eat large numbers of mos- quitoes (Whitaker & Lawhead 1992). The few previous exceptions to this trend are Holarctic species (Anthony & Kunz 1977, Kurta & Whi- taker 1998, Shiel et al. 1998). Our data indicated that H. speoris captured many mosquitoes at Si- giriya. We expect that other tropical bats foraging on insects above water bodies at dusk and dawn would also consume large numbers of mosquitoes.

Twilight Foraging by Bats 679

Hipposideros speoris is one of many tropical bats that preys on swarms of nuptial termites and ants (Whitaker & Black 1976, Eckrich & Neu- weiler 1988, Kunz et al. 1995, Rydell & Yalden 1997). Such swarms may be a particularly prof- itable food source for insectivores because they are concentrated in space and time and individuals contain large quantities of stored nutrients (Wat- son & Gay 1991). The availability of these taxa, however, can be highly seasonal and this is reflect- ed in marked changes of their presence in bat diets across sampling periods (LaVal & LaVal 1980, Whitaker et al. 1999). For example, Indian pygmy bats (Pipistrellur mimus) captured termites during only 3 of 24 fortnightly sampling periods, but ter- mites made up 48.4 and 59.5 percent by volume of fecal samples during two of these periods (Whi- taker e t al. 1999). The seasonality in termite and ant predation shown by bats contrasts with ter- restrial and fossorial mammals, many of which are specialized ant and termite predators (Redford 1987).

We used a combination of fecal and prey re- mains samples to assess the diet of the study colony. The inclusion of insects identified among prey re- mains has increased our understanding of both the taxonomic and size range of prey captured by H. speoris during twilight activity. Prey remains analysis is biased toward large insects, the body parts of which bats selectively cull before feeding (Rabinow- ia & Turtle 1982, Jones 1990). We identified such a bias in our study (Fig. 2); however, we consider fecal analysis also to be biased, because small wings are more likely to remain intact as they pass through a bat's digestive tract than medium-sized wings, which are chewed rather than swallowed whole. As

a consequence, when prey size is determined based on length of intact wings in feces, only small prey items will be included. Therefore, we believe that the use of both methods would be more accurate in determining the prey-size range of insectivorous bats than either one alone.

In summary, our study has established that twi- light activity provided the members of a maternity colony of H. speoris in Sri Lanka with access to in- sects that were either nor available or not present in such high abundances during true night. In deciding when to emerge from a roost, individual H. speoris face a trade-off between the dietary benefits of for- aging on these insects and the increased risk of being caught by a predator during twilight. Our study oc- curred during pregnancy and lactation when nutri- ent and energy requirements of female bats are high, and therefore, when they are expected to take higher risks. We did not study the activity and dietary pat- terns of the colony during the non-reproductive pe- riod that coincides with the monsoon season in cen- tral Sri Lanka. Insect abundance would be far greater following heavy rain, and activity patterns of the colony could be markedly different.

ACKNOWLEDGMENTS The project was completed while the senior author was a recipient of a Research Fellowship from the Alexander von Humboldt Foundation. Research was carried out with the permission and support of the Department of Wildlife Conservation of the Government of Sri Lanka (especially Mr. H. D. Ratnayake, Deputy Director, Re- search and Training) and the Central Cultural Fund. We thank Sujeewa Jasinghe for assistance with organization and fieldwork and the staff of Sigiriya Rest House for their help during our stay. R. Mark Brigham, Jens Rydell, and two anonymous referees provided very helpful com- ments on earlier draks of the manuscript.

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