American Society of Mammalogists

Seasonal Foraging Behavior of the Frugivorous Bat Carollia perspicillata Author(s): Theodore H. Fleming and E. Raymond Heithaus Source: Journal of Mammalogy, Vol. 67, No. 4 (Nov., 1986), pp. 660-671 Published by: American Society of Mammalogists Stable URL: http://www.jstor.org/stable/1381127 Accessed: 18/05/2010 07:51
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SEASONAL FORAGING BEHAVIOR OF THE FRUGIVOROUS BAT

CAROLLIA PERSPICILLATA
THEODORE H. FLEMING AND E. RAYMOND HEITHAUS Department of Biology, University of Miami, Coral Gables, FL 33124 (THF) Department of Biology, Kenyon College, Gambier, OH 43022 (ERH)
ABSTRACT.-We studied the foraging behavior of the frugivorous bat Carollia perspicillata (Phyllostomidae) during two dry seasons and two wet seasons in northwestern Costa Rica using radio-telemetry and capture-recapture techniques. Seasonal changes occur in both quantitative and qualitative aspects of this bat's foraging behavior, primarily as a result of changes in the density and distribution of food. Compared to bats in the wet season, bats fly greater distances to harvest fruit, are concentrated in fewer resource patches, change general feeding locations more frequently, and are more sensitive to moonlight conditions in the dry season. In both seasons, bats show high short-term fidelity to the 2-3 feeding areas they visit each night. Food distributions, predatorrisk, and, in males, social status, influence the foraging behavior of C. perspicillata.

The foraging behavior of many bats changes seasonally. Seasonal changes in types of prey eaten, night roosting behavior, and intensity of foraging effort are ubiquitous in temperate zone hibernating species (Anthony and Kunz, 1977; Anthony et al., 1981; Barclay, 1982; Davis and Hitchcock, 1965; Erkert, 1982; Humphrey et al., 1977; Kunz, 1974; O'Shea and Vaughan, 1977; Stebbings, 1968; Tuttle, 1976). In tropical bats, seasonal changes are known to occur in the following foraging parameters: diet breadth and type of food, patterns of habitat use, defense of feeding areas, foraging group size, and migratory behavior (Barclay, 1985; Bonaccorso, 1979; Bradbury, 1977; Bradbury and Vehrencamp, 1976; Fenton et al., 1985; Fenton et al., 1977; Heithaus et al., 1975; Lemke, 1984; Start and Marshall, 1976; Thomas, 1983; Thomas and Fenton, 1978; Vaughan, 1976; Whitaker and Black, 1976). All or most of these behavioral changes ostensibly reflect seasonal changes in climate and the availability of suitable food items. In this paper we examine seasonal changes in the foraging behavior of the common neotropical frugivorous bat, Carollia perspicillata (Phyllostomidae), by addressing the following questions: (1) Are there qualitative or quantitative seasonal differences in the foraging behavior of C. perspicillata? (2) Within seasons, do significant year-to-year changes occur in its foraging behavior? (3) What is the relative importance of food distribution, predation risk, and social status as factors affecting its foraging behavior? To answer these questions we studied the foraging behavior of C. perspicillata during two dry seasons in northwestern Costa Rica and compared our results with those of a similar study conducted during two wet seasons at the same site (Heithaus and Fleming, 1978). STUDYAREAAND METHODS This study was conducted in Parque Nacional Santa Rosa, Guanacaste Province, Costa Rica, from midJanuary to mid-to-late March in 1977 and 1978. The study area lies in the Tropical Premontane Moist Forest life zone (Holdridge, 1967) at an elevation of about 300 m. Santa Rosa consists of a mosaic of forest patches of various successionalstages and fire-maintained grasslands;its vegetation is described in detail by Hartshorn(1983). In upland parts of the park where we worked, seasonally-deciduoustropical dry forest is the major habitat. Widely scattered patches of evergreen forest occur in moist ravines in the uplands and are more extensive in the park's lowlands. Rainfall is highly seasonal and virtually all of the annual total (about 1,600 mm) falls between early May and mid-November. Our study was conducted at the height of the dry season when most tree species were leafless. Our previous study was conducted in June through August of 1975 and 1976 during the first half of the wet season after the forest canopy had completely leafed out. We used radiotelemetry to study the foraging movements of 26 individuals of C. perspicillata, 12 (11 males and one female) in 1977 and 14 (10 males, four females) in 1978. None of the females was reproductively active. These individuals were captured in mist nets as they left the Sendero Cave just after sunset
J. Mamm., 67(4):660-671, 1986

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(see Heithaus and Fleming, 1978). The weights of radio-tagged bats ranged from 18.5 to 21.5 g in 1977 and from 17.0 to 24.0 g in 1978. We attached an AVM-SM1 transmitter equipped with a battery and antenna (2 g total weight) to the back of each bat with Silastic medical adhesive. Transmittersremained on these bats for an average of 11.7 days (range = 4-19 days) in 1977 and 10.6 days (range = 5-22 days) in 1978. We tracked the bats using triangulation and other techniques as described in Heithaus and Fleming (1978) for 4-5 h on an average of 10.4 nights (range = 3-18 nights) and 7.8 nights (range = 3-17 nights) in 1977 and 1978, respectively. To determine the relative densities of bats in various areas away from the roost and to obtain dietary information (Heithaus et al., 1975), we captured bats in mist nets, collected fecal samples, and banded them on one forearm with a numbered plastic band (A. C. Hughes, Ltd., Hampton Hill, England). In 1977 we dusted 38 individuals with a cube of pollen gel (Beattie, 1971) and examined the melted gel under a compound microscope for evidence of flower visitation. Stashko (1982) similarly dusted 76 individuals for pollen in 1978. Additional data that are relevant to this comparison have been collected since 1978. These studies include radio-tracking 40 bats during the summers of 1980 and 1981, studies of the social organization of C. perspicillata in 1980 and 1981, and a year-long capture-recapture and plant phenology study in 1983 and 1984. Detailed results of these studies have appeared (Williams, 1986) or will appear elsewhere. Whenever possible, we used the methods of Heithaus and Fleming (1978) to summarize and analyze our radio-tracking data. Our goal was to determine as precisely as possible the following foraging parameters: (1) number and location of each bat's feeding areas (hereafter abbreviated as FAs), which we have previously defined as any area in which a bat remains for at least 30 min; (2) rates of movements between FAs; (3) night-to-night consistency in the use of FAs; and (4) total distance flown each night. We often had difficulty in measuring these parameters precisely, because compared with individuals in our wet season study, bats generally were a long distance (>1 km) from our receiving stations. Together with our measured error margin of 5-6% in accurately determining the known locations of transmitters,long distance triangulations caused our data plots of feeding locations to be spread out over a greater area than was the case with the wet season data. Our dry season triangulation data, therefore, sometimes made it difficult to resolve nearby FAs and to quantify rates of movements between them. Owing to seasonal differences in resolution, we have attempted to be conservative in the identification of spatially-distinct activity areas (i.e., FAs). For the 1977 data, Fleming used a combination of field plots of triangulation data made the day after a tracking session and computer-drawn maps to define the locations of FAs. Heithaus worked with hand-drawn maps after the 1978 field season. We identified FAs on the basis of two criteria: (1) a reasonably tight cluster of points, and (2) repeated visits to these areas on two or more nights. We ignored outlying points and small clusters of points that appeared only on one tracking night if there were multiple-night clusters nearby on the assumption that these points were "noise" in the data. To determine distances between FAs and the roost, we measured from the center of each cluster of points to the center of other FAs or to the roost. Because bats often did not fly in a straight line between FAs and to and from the roost, these measurements must be considered minimum estimates of the distances bats actually flew.

RESULTS

Food Habits and Food Availability Our previous work in Guanacaste Province (Heithaus et al., 1975) indicated that C. perspicillata eats fruit and visits flowers for nectar in the dry season, whereas it is exclusively frugivorous (and, to a minor extent, insectivorous) in the wet season. Our early wet season food habit data at Santa Rosa (Heithaus and Fleming, 1978) indicate that the bulk of its diet comes from fruits produced by the shrub species (Piper amalago, P. pseudo-fuligineum, and P. jacquemontianum and fruits of the tree species Muntingia calabura, Cecropia peltata, and Chlorophora tinctoria. With the exception of P. jacquemontianum, which is restricted to patches of evergreen forest (Fleming, 1985), each of these species is common, but patchily-distributed, in deciduous and evergreen forests. Estimates of the nightly ripe fruit biomass of these species in the wet season range from 12 to 45 kg per ha in suitable habitats (Heithaus and Fleming, 1978). In the dry season at Santa Rosa, C. perspicillata is mainly frugivorous but occasionally visits flowers of two species of canopy trees. Characteristicsof its dry season diet are summarized in

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TABLE 1.-Summary of general characteristics of the diet of Carollia perspicillata in the dry season. Sources of data include Fleming (1985), Heithaus and Fleming (1978), and Stashko (1982). General importance in diet Habitat' and density (no. plants per ha)

Family and species

Period available

A. Fruit species Piperaceae Piper marginatum P. amalago P. jacquemontianum P. tuberculatum Elaeocarpaceae Muntingia calabura Moraceae Cecropia peltata Leguminosae Acacia collinsii Rhamnaceae Karwinskia calderoni Melastomataceae Clidemia octona Chrysobalanaceae Licania arborea Guttiferae Vismia baccifera Bombacaceae Bombacopsis quinatum Minor Jan-Feb D Minor Major Major Major? Minor Minor April-Oct March-May Jan-Feb Jan-March March April-May B. Flower Species (common) D, E, R D, E D, R E D E (5-100) (20-300) (1-2) (low) (3-4) (low) Major Minor Major Minor Major Jan-Feb Feb-March March-April April-May Feb-July D, E D, E E R D, E (100-300) (100-200) (100-200) (low) (10-500)

Ceibapentandra

Minor

Jan-March

(rare)

a Habitat abbreviationsare: D = deciduous forest, E = evergreen forest, R = riparian forest.

Table 1. With the exception of P. jacquemontianum, none of its wet season fruits are major components of its dry season diet. Compared with wet season fruits, species eaten in the dry season tend to have shorter fruiting periods (which leads to higher turnover rates in month-tomonth diet composition in the dry season than in the wet season), and many of them are restricted in distribution to moist habitats (i.e., evergreen or riparian forests). Only Acacia
collinsii and Piper marginatum are common plants in deciduous habitats. Nightly biomass of ripe fruits (<1-11 kg ha-1) is lower in the dry season than in the wet season.

Our data and those of Stashko (1982) indicate that C. perspicillata apparently does not visit flowers frequently at Santa Rosa. In 1977, 17 of 38 bats (45%) tested were carrying pollen on
their fur; 11 individuals were carrying Ceiba pentandra pollen, two were carrying Bombacopsis

quinatum pollen, and four bore a mixture of Ceiba and Bombacopsis pollen. Stashko (1982) reported that only 7% (n = 76) of the bats he tested were carrying pollen (all B. quinatum). Whereas B. quinatum flowers annually, C. pentandra does not flower every year (D. Janzen, pers. comm.). The proportion of individuals carrying pollen differed significantly in 1977 and 1978 (x2 = 19.24, d.f. = 1, P < 0.001). This difference can be attributed to the availability of C. pentandra flowers in 1977 but not in 1978. In summary, seasonal changes in food availability in Santa Rosa are substantial and lead to the following predictions regarding seasonal differences in the foraging behavior of C. perspicillata. Compared with the wet season, it should (1) forage farther away, on average, from its day roost, (2) visit more FAs per night, (3) concentrate its feeding activity in a narrower range of habitats, and (4) change the locations of its FAs more frequently as new fruits come into season.

TABLE 2.-Summary of the foraging behavior of Carollia perspicillata in four seasons. The 1975-76 data com noted, values are means and ranges (in parentheses). Parameter 1975-76 (wet)

19

Consistency of roost use (proportion) Total known feeding areas (=FAs) Number of FAs visited per night Distance from cave to FAs (km) Nightly FA overlap, within individuals FA overlap between individuals Distance between an individual's FAs (km) Rate of movement between FAs (no. moves/h) Minimum distance flown/night (km)
a95% confidence limit of items. bStandarddeviation. * Subjective estimate (see Fig. 2).

0.86 4.1 (2-6) 2.2 (0.33)a 0.94 (0.1-3.2) 0.70 (0.19)b 0.0025 0.65 (0.14)p 0.65 (0.46-0.82)a 7.24

0.69 4.2 ( 2.1 ( 1.41 0.67 0.30 1.31 0.71 12.3

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of bats roost of FIG. 1.-Map of the locations feedingareasof radio-tagged in 1977.Location the Sendero individuals. The is indicated the solidtriangle.Uppercase letterssignifythe feedingareasof different by areasare patchesof forest; bareareasare abandoned pastures. stippled

Foraging Behavior A quantitative summary of the foraging behavior of C. perspicillata based on four seasons (two wet and two dry seasons) of fieldwork is presented in Table 2. We discuss these data and our qualitative observationsbelow. Consistency of roost use.-Individuals are highly faithful to a single day roost (i.e., the Sendero Cave) in both wet and dry seasons. The probability of an individual returning to the Sendero Cave each morning ranged from 0.69 (72/105 bat-mornings) in the 1977 dry season to 0.86 in the wet seasons of 1975 and 1976 (Table 2). The failure of some individuals to return to their regular day roost probably reflects a response to the trauma of being radio-tagged. In

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FIG. 2.-Map of the locations of feeding areas of radio-tagged bats in 1978. Upper case letters signify the feeding areas of different individuals. Other symbols as in Fig. 1.

each field season, a few individuals temporarily moved to an alternate roost for a few days immediately after being radio-tagged. Most of these bats eventually returned to the Sendero Cave. Number and locations of individual feeding areas.-Regardless of season, bats visited from one to eight different FAs during their tracking tenure. On a given night, individuals visited, on average, two or three of these FAs. Bats had visited a majority (90% and 72% in 1977 and 1978, respectively) of their known FAs by their third tracking night in the dry season just as they had in the wet season (Heithaus and Fleming, 1978). There were no obvious seasonal differences in total number of known FAs or number of FAs visited per night (Table 2). The general locations of FAs changed seasonally to some extent. In the wet season, most bats

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living in the Sendero roost foraged in deciduous forest north of the roost;a minority of individuals (ca. 20% of all wet season individuals we have tracked) foraged either east or south of the roost (Heithaus and Fleming, 1978 and more recent data). In the 1977 dry season, in contrast, most individuals foraged northwest or south of the Sendero roost (Fig. 1). Prior to 15 February, most (20/21) known FAs were north or northwest of the roost;after 15 February, most (15/19) of the known FAs were located south of the roost. The location of the 1978 FAs more closely resembled the distribution of wet season FAs in that most individuals foraged either north or south of the roost (Fig. 2). No strong intra-seasonalshift in foraging locations occurred in 1978. A higher proportion (58%, n = 26) of Sendero individuals foraged south of the roost, often outside the park boundaries, in the dry season than in the wet season (x2 = 9.19, d.f. = 1, P < 0.05). Distance between the day roost and all FAs.--This parameter indicates the average straightline distance that a bat must commute between its roost and its first FA. Mean values for 197576 and 1978 were similar and were about 40%lower than the 1977 value (Table 2). Differences between these means are statistically significant (Kruskal-WallisAnova, X2 = 10.98, d.f. = 2, P = 0.0041). During most of the year, most individuals commute no more than 1 km from roost to first FA, but a few individuals commute over 3 km to their first FA. Variationin this foraging parameter bears no obvious relationship to bat size (controlling for social status in males) (Heithaus and Fleming, 1978), but netting studies (e.g., Stashko, 1982) indicate that females tend to forage farther from the day roost than males. The high mean value in 1977 (1.4 km, cf. 0.8 km in other field seasons) reflects the effect that an irregularly-availableresource (flowers of Ceiba pentandra) has on C. perspicillata's foraging behavior. Consistency in the use of FAs.-Regardless of season, individuals are highly consistent in their use of a set of FAs. They return to the same FAs night after night as long as an adequate food supply can be found there. We quantified night-to-night consistency by calculating mean pairwise nightly overlap in the circular distributionof tracking recordsat particularbase stations using Pianka's (1974) symmetrical overlap index as explained in Heithaus and Fleming (1978); we used 20? blocks in these calculations as conservative measure of the accuracy of our tracking system. Night-to-night consistency within individuals averaged 0.67-0.70 (out of a maximum value of 1.0) in the 1976 and 1977 tracking seasons (Table 2). Although we could not calculate mean overlap in 1978, qualitative observationsindicate that it was also high. FA overlap between individuals.-Similar calculations can be made to quantify spatial overlap between individuals. By taking into account temporal (i.e., nightly) and spatial overlap, Heithaus and Fleming (1978) documented that FA overlap is very low in the wet season (Table 2). Less detailed data in 1977 precluded weighting spatial overlap by a temporal factor so that estimates of between-individual FA overlap made in 1976 and 1977 are not equivalent. Nevertheless, the 1977 calculation of between-individual overlap, though lower than the estimate of within-individual (nightly) overlap, is considerably higher than the wet season value (Table 2). Inspection of Fig. 2 reveals that inter-individual FA overlap also was relatively high in the 1978 dry season, especially in areas < 1 km from the roost. Netting data also indicate that the FAs of different individuals overlap extensively in the dry season. In February 1977, for example, 62 individuals of C. perspicillata were captured in 54.0 net-hours at the site marked Laguna northwest of the Sendero roost (Fig. 1). This capture rate (1.15 bats per net-hour) is about twice as high as the typical wet season non-roost capture rate of ca. 0.54 bats per net-hour. The Laguna site was sampled again in March 1977 after bats had shifted their FAs, and the capture rate was 0.12 bats per net-hour (three Carollia in 24.8 nethours). Similar high FA overlap both within and between roosts in the dry season was documented in the extensive netting program in 1983-84. Nightly flight distances.-Data needed to calculate total nightly flight distances include commute distances (i.e., the distance between the roost and the first and last FA visited each night), distances between the FAs visited on a given night, the rate of movement between FAs, and the distances flown between night roosts and sources of food within FAs (Heithaus and

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Fleming, 1978). Since we rarely tracked individuals continuously for entire nights, we cannot present actual data on flight distances. Instead, we rely on average values of tracked individuals to estimate the (minimum) distance flown by bats each night; most of the values needed for these calculations are shown in Table 2. in Nightly flight distance was calculated as 2C + DbFA + DWFA which C = mean commute distance (i.e., average distance between the roost and all FAs), DbFA = distance flown between FAs, and DWFA= distance flown within FAs as bats harvest fruit and carry them to a night roost
(see Heithaus and Fleming, 1978). DbFAwas calculated as 7(RbFA)(MbFA) in which 7 represents

an estimate (based on evening and morning tracking sessions of the same bat) of the average time (in hours) that a bat spends away from its day roost, RbFA= the rate of movement between is was FAs, and MbFA the mean distance between FAs (Table 2). The calculation of DWFA based on the harvest of 30 fruits (bats harvest more fruits than this when eating Piper and less fruits when they eat Chlorophora or Cecropia fruits) times a flight distance of 80 m between night roost and fruit source in the wet season and 100 m in the dry season (see below, Return to day roost). Results of these calculations (Table 2) indicate that an "average" bat usually flies a minimum of about 7-8 km per night. Nightly flight distances in 1977 were nearly twice this value because of the longer commute distances and greater distances between FAs. The proportional contribution of the major components of flight varied relatively little between seasons and years and averaged 19.8% (commutes), 44.6% (moves between FAs), and 32.6% (harvesting fruit within FAs). As previously noted, these calculations are minimum estimates of actual flight distances because they are based on straightline measurements between destinations. The actual distances flown while commuting or moving between FAs were often longer than this because bats usually avoided flying over open grassland and instead traveled through forest when changing sites. A second reason why our calculations minimize flight distances, especially in the dry season, is that some bats occasionally used the Sendero Cave as a night roost. In the wet season, only harem males and other individuals feeding close to the cave used the day roost as their night roost (Heithaus and Fleming, 1978; Williams, 1986). In contrast, a greater number of individuals, including those feeding > 1 km from the cave sometimes returned to the cave between feeding bouts during the dry season. In 1977, four of 12 bats made relatively long-distance moves back to the cave on 13 occasions. In 1978, six of eight individuals made similar moves on 23 out of a possible 44 nights. These returns to the day roost greatly elevate the total distance that bats fly when they are harvesting fruit in the dry season. If these longer moves had been fully accounted for in calculations of total flight distances in 1977 and 1978 (Table 2), dry season flight distances would certainly exceed those in the wet season, and the proportion of total flight represented by travel between fruit sources and night roosts would be higher in the dry than in the wet season. Exploratory flights and rates of change of FA locations.-Because the locations of suitable feeding sites change through time, bats need to spend some time and energy looking for new FAs. Exploratory behavior is difficult to define operationally, and we have been conservative in identifying such flights. Heithaus and Fleming (1978) reported that these flights represented only 1.5%of the estimated 393 km moved by the bats they tracked. We cannot estimate the frequency of exploratory flights in our dry season bats, but one 1977 bat (individual D in Fig. 1) provided us with a clear picture of how bats are likely to shift from an old FA to a new one. Between 11 and 18 February this female foraged northwest of the roost as was the case for the bulk of our radio-tagged bats (Fig. 1). Before flying to her northwest FA(s) at 2215 on 20 February, she flew 1 km southeast of the roost (site X in Fig. 1) and was active there for three hours. On 21 February, she spent 1.3 hrs in the southeast area before flying to the northwest. She foraged in the northwest on the morning of 23 February, but remained in a new area farther south of the roost (site * in Fig. 1) until at least 2300 that night. On 24-25 February, she was in the south from 1830 to 1940 and then spent the rest of

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28----*----

26_

25 ..:
23.
< .{......IiI.II,--.

_ .....-

22

m 21.
Ui. 19
0 18^ * __ _

_
___

I-17
Fb15 . The m- on..... ....ll ..
n o

of

-F

14e 3igthe

nlight On25

and 27 _

reFebruary e

._

7. bars_

indicate the time of darkness (both sun and moon below the horizon). Solid lines indicate times that a bat
was in the Sendero February. The moon roost. Bat #051028 was monitored of 22 February. on all nights; its activity is shown just above the

"darkness bars." Bat #031028 was monitored from 11 to 19 February and bat #122128 from 22 to 28
was full on the night

the night in the northwest. On 25 and 27 February she remained south of the roost during the time she was tracked, and her transmitter fell off in her south FA on 28 February. In summary, this individual gradually changed the location of her feeding site over a period of days by visiting the new site(s) early in the evening before flying to her old site(s). Bats probably continue returning to a set of FAs as long as possible in both the wet and dry seasons. The relatively short residence time of the transmitter on a bat's back (2-3 weeks) prevents us from directly measuring how long a set of FAs is used. The 1983-84 netting program, however, gives us additional insight into this matter. In the 1983 wet season, for example, the probability that a bat captured in a resource patch would be recaptured in the same patch one month later was 0.67 (n = 51 bats), whereas it was only 0.39 (n = 52 bats) in the 1984 dry season. These differences are statistically significant (X2 = 8.21, d.f. = 1, P < 0.05) and are consistent with our prediction that bats should change feeding locations at a higher rate in the dry season than in the wet season.

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Activity rhythms and the response to moonlight.-In both the wet and dry seasons, the activity of radio-tagged individuals, as measured by tallying the proportion of 15 minute time blocks containing one or more actively moving bats during all tracking sessions,was high (0.500.60) early in the evening (between sunset and ca. 2100) and again from ca. 0230 to sunrise; activity levels were lowest in the middle of the night (Heithaus and Fleming, 1978). In the wet season, general levels of activity were not depressed on moonlit nights, but the distance that bats moved between FAs was negatively related to levels of moonlight (Heithaus and Fleming, 1978). The average moving distance on bright nights was only 21% of the distance moved on dark nights. Moonlight had a strong effect on activity levels and timing of feeding during the dry season. For example, general activity levels were significantly lower during the first half of the night on moonlit nights (x = 0.37 ? 0.09 SD) than on dark nights (f = 0.43 ? 0.12) (Binomial Test, n = 18, P = 0.004); levels of moonlight did not influence activity levels during the last half of the night (Binomial Test, n = 15, P = 0.85). Bats sometimes stayed in the cave when the moon was above the horizon early in the evening and did not leave to feed until the moon was down (Fig. 3). Intermittent returns to the cave from distant FAs, however, were no more frequent during the bright half of the month (n = 6 instances in 1977) than during the dark half (n = 7 instances in 1977).
DISCUSSION

Based on knowledge of seasonal changes in the abundance and distribution of food (fruit and flower) resources, we predicted that during the dry season individuals of C. perspicillata should (1) forage farther away from their day roost, (2) visit more FAs per night, (3) concentrate their feeding activity in a narrower range of habitats, and (4) change the locations of their FAs more frequently than in the wet season. Our radio-tracking and more recently-obtained mist netting results indicate that predictions (1), (3), and (4) are likely to be correct. Because a higher proportion of bats fly south to woodlots off park property in the dry season, average commute distances probably are longer than in the wet season. (Calculations of average distance between the Sendero roost and known FAs (Table 2) did not take these long commutes into account because the locations of FAs outside of the park were not precisely known.) Commute distances were significantly longer in 1977 than in either 1975 or 1976. Bats forage in a variety of habitats, including deciduous, evergreen, and riparian forests in both seasons but, based on the results of mist-netting studies, they tend to be concentrated in fewer resource patches in the dry season. Bats also appear to shift the locations of their FAs more frequently, presumably in response to a higher rate of food species turnover per month in the dry season. Finally, the activity of bats appears to be more strongly influenced by moonlight conditions in the dry season. At least two important features of the foraging behavior of C. perspicillata do not appear to change seasonally, namely the number of FAs that an individual visits each night and the high night-to-night consistency with which bats visit a given set of FAs. These unchanging aspects of foraging in C. perspicillata indicate that individuals use the same qualitative foraging strategy year-round. This strategy involves concentrating on fruit species of low nightly density but high spatio-temporal predictability whenever possible to minimize the energetic costs of commuting and searching for food. A similar strategy is used by the phyllostomid Phyllostomus hastatus on Trinidad (McCracken and Bradbury, 1981). In contrast, Artibeus jamaicensis concentrates on ephemeral but abundant fruit species (e.g., Ficus species) on Barro Colorado Island, Panama (Morrison,1978a). Based on radio-tracking data from four wet seasons and two dry seasons, it appears that the wet season foraging locations of bats roosting in the Sendero Cave are more similar year-to-year than are the locations of dry season foraging areas. Only in the dry season of 1977 have we seen Sendero bats foraging in numbers west of the roost. In other seasons, most individuals forage either north or south of the roost. Although we do not know precisely why bats were foraging west of the roost in 1977, it likely was related to the availability of flowers of Ceiba pentandra, a favorite nectar source of C. perspicillata and other non-specialized flower visiting bats during

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the dry season in northwestern Costa Rica (Heithaus et al., 1975). We netted individuals of C. perspicillata bearing pollen of C. pentandra at two sites in 1977: near the Sendero roost (within 100 m of a flowering individual) and at the Laguna site (Fig. 1). We assume that bats bearing Ceiba pollen at Laguna obtained the pollen at that site rather near the roost before flying west. Whatever the reason for the high concentration of bats in the Laguna area in February 1977, this shift in foraging locations markedly increased the average commute distances of bats in that season compared to other seasons and years. The intermittent return of many individuals to the day roost also increased overall flight distance in the dry season. This behavior was seen in males and females and did not always occur on moonlit nights. These returns do not appear to be associated with increased social activity in the roost during the dry season (Williams, 1986). We do not know why bats make long flights back to the roost before they have finished feeding but speculate that it is related to predator avoidance. If correct, this hypothesis implies that the cost of these irregular flights is less, in terms of energy expenditure and exposure to predators, than is the regular use of one or more night roosts located closer to food sources. The most plausible reason why this might be so is that safe night roosts are much scarcer in the dry season when many parts of the forest are leafless. Another indication that predation risk outside the roost is higher in the dry season than in the wet season is the response of C. perspicillata to bright moonlight. In our experience, it is unusual for bats to delay departure from the day roost much beyond 0.5 h after sunset in the wet season. Most bats promptly leave the roost, regardless of time of month or weather conditions, near sunset at that time of the year (Heithaus and Fleming, 1978). In contrast, in dry season many individuals delay their departure or return to the day roost during periods of bright moonlight (Fig. 3). Since fruit availability is not affected by moonlight, the only plausible explanation for this behavior is that it reduces the exposure of C. perspicillata and other frugivorous (and sanguinivorous)bats to predators (Morrison,1978b; Wilkinson, 1985). In conclusion, the foraging behavior of C. perspicillata appears to be sensitive to at least three major factors: the abundance and distribution of food, exposure to predators, and social status. Characteristicsof the food supply influence where bats feed, how long they return to the same set of FAs, and how often they need to search for new FAs. Avoidance of predators influences the bats' choices of night roosts and their activity periods, especially during the leafless portion of the dry season. Finally, although not a topic of this study, the social status of males (harem males vs. bachelor males; Porter, 1979) influences their foraging behavior. Harem males forage closer to the day roost and use this roost as their night roost on most nights throughoutthe year, whereas bachelor males, like females, forage at various distances away from the day roost throughout the year (Williams, 1986). The relative importance of these factors appears to be: food distribution > predator risk > social status.
ACKNOWLEDGMENTS

It is a pleasureto acknowledge CostaRicanNationalParkService(AlvaroUgalde,Director)for the SantaRosaandthe parkpersonnel theirsupport hospitality. for to Nacional and permission workat Parque Field assistance providedby Pat Skerrett, and was MichaelZimmerman, SandyMcRaein 1977 and Ed in PamelaAnderson, Richard Stovel,andDebbieShields 1978.Barbara Stashko, Schneider computer-coded the 1977data.Neil Gillieswrotethe computer that mostof the 1977radio-tracking program summarized data.Thisresearch supported NSFgrantsDEB 75-23450and DEB 78-26493.Thispaperis Contriwas by butionNo. 224 from the Program Ecology,Behavior, in and TropicalBiology,Department Biology, of of University Miami.
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