Bonaccorso and gush, 1987.pdf

Feeding Behaviour and Foraging Strategies of Captive Phyllostomid Fruit Bats: AnExperimental StudyAuthor(s): Frank J. Bonaccorso and Thomas J. GushReviewed work(s):Source: Journal of Animal Ecology, Vol. 56, No. 3 (Oct., 1987), pp. 907-920Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/4956 .Accessed: 11/01/2013 13:23

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Journal of Animal Ecology (1987), 56, 907-920

FEEDING BEHAVIOUR AND FORAGING STRATEGIES OF CAPTIVE PHYLLOSTOMID FRUIT BATS:

AN EXPERIMENTAL STUDY BY FRANK J. BONACCORSO* AND THOMAS J. GUSH

Department of Biology, University of Miami, Coral Gables, FL 33124, U.S.A. and Ecology and Evolution Department, State University of New York,

Stony Brook, NY 11794-5254 U.S.A.

SUMMARY

(1) Feeding rhythms, rates, and fruit selectivity were observed in flight cage experiments involving seven species of frugivorous bats (Chiroptera: Phyllostomidae) from two distinct foraging guilds: canopy frugivores specializing on superabundant fruits of canopy trees and groundstorey frugivores specializing on fruits of shrubs and understorey trees of low fecundity.

(2) Bat species differed in handling times of individual fruits, feeding rhythms, and fruit species selectivity with groups of bat species corresponding to previously defined guilds. Canopy frugivores fed continuously throughout most of the night and ate each fruit slowly. Groundstorey frugivores fed in a series of discontinuous bouts separated by periods of roosting/sleeping and ate individual fruits rapidly.

(3) Bat species differed in cumulative food item feeding rates over 2-4 h experimental periods, but species subsets did not correspond to established guilds.

(4) Paired fruit choice tests showed that captive bats selected fruits that wild populations of their species commonly eat. Groundstorey frugivores selected fruits high in nutrient content. Canopy frugivores selected familiar fruits of low nutrient content over nutritionally higher quality fruits that wild conspecifics rarely eat.

(5) Exploitation competition for some limited food resources is discussed as a possible mechanism that has led to resource partitioning and foraging specialization in neotropical bat communities.

INTRODUCTION

The neotropical bat family, Phyllostomidae, includes a large number of frugivorous species (Gardner 1977). Many of these bat species in the subfamilies Carollinae, Stenoderminae, and Glossophaginae are obligate frugivores much of the year, but seasonally feed on nectar/pollen and/or insects (Heithaus, Fleming & Opler 1975; Bonaccorso 1979). The degree and frequency of switching among food items depends on the relative abundance of food resources and competitors, and thus is temporally and geographically variable (Humphrey & Bonaccorso 1978).

* Present address: Department of Zoology and P. K. Yonge Laboratory School, University of Florida, Gainesville, Florida 32611 U.S.A

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Fruit bat feeding/foraging All phyllostomid frugivores forage solitarily, usually remove fruits from plants, and

then consume picked fruits 5-100 m away in small trees or vine tangles termed feeding roosts (Dalquest 1954; Goodwin & Greenhall 1961; Janzen et al. 1976; Morrison 1978a, 1980; Bonaccorso 1979; Fleming 1982). These bats feed in the fruit-bearing trees only in exceptional instances when fruits are too large or too firmly attached to carry away (Bonaccorso, Glanz & Sandford 1980). Throughout a night, an individual bat consumes more than its own weight in fruit, harvests 10-80 fruits, and commutes among the day roost, one or more resource patches, and feeding roosts (Morrison 1978a; Heithaus & Fleming 1978). Feeding patches may include a single large tree or a large number of shrubs and are used repeatedly until fruit production diminishes (Heithaus & Fleming 1978; Fleming 1982). Scouting flights occasionally are taken to assess the status of ripening fruit crops in potential feeding patches throughout the home range during dark periods of the night when predation risk is minimal (Morrison 1978a, b; Fleming 1982).

Virtually all frugivorous phyllostomids can be placed into one of two feeding guilds described by Bonaccorso (1979). Members of the first guild, canopy frugivores (most Stenoderminae), specialize on the massive fruit crops of canopy level trees, 10-30 m in height. As a consequence, most of the foraging activity of these bats occurs well above ground level (> 3 m) and within primary forest (Bonaccorso 1979). Bats in the second feeding guild, groundstorey frugivores (Carollinae and, during seasons when they are frugivores, some Glossophaginae), specialize on the fruits of shrubs and understorey trees (0 1-3.0 m in height) that produce small to medium fruit crops. These bats mostly forage close to ground level ( < 3 m) and are most abundant in early successional stages leading to primary forest, but also forage in the understorey of primary forest (Bonaccorso 1979). Fleming (1982) and Heithaus (1982) review the foraging strategies and bat-plant interactions involving these and other fruit bats.

This paper presents comparative data on the feeding behaviour of frugivorous phyllostomid bats in Parque Nacional de Santa Rosa, Costa Rica, using controlled experiments and observations in large outdoor flight cages. Many of the field studies published on bat ecology have used indirect techniques such as radiotelemetry and mist- netting to gather data for inferring ecological patterns. It is rarely possible to directly observe the feeding behaviour of wide-ranging frugivorous bats, even in situations which permit use of night vision devices to observe bats picking fruits, because the bats carry fruits to unpredictable sites and frequently change their feeding roosts. Controlled experiments with captive bats as used in this study make it possible to isolate behavioural phenomena associated with feeding behaviour and foraging strategy that otherwise could not be observed with presently available techniques. In the discussion that follows, we amalgamate the data on captive bats from this study with the published information on field ecology, which is extensive for several species included here. When possible we indicate where our observations are corroborated by field data.

We ask the following questions about fruit bats of the canopy and groundstorey foraging guilds. (i) Do bats feed continuously or discontinuously through the night? (ii) How long does it take to handle individual fruits? (iii) At what rates do bats eat successive food items? (iv) How much of the nightly time budget is occupied with feeding? (v) Do fruit bats act as time minimizers or energy maximizers sensu Schoener (1971)? (vi) Are captive bats selective or do they feed randomly if given a choice of ripe fruits known to be selected by free-roaming bats in Santa Rosa? (vii) How do the observed behavioural patterns correlate with abundance, biomass, and spatiotemporal dispersion of fruit resources in molding foraging strategies of these bats in Santa Rosa?

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F. J. BONACCORSO AND T. J. GUSH METHODS

This study took place between 15 May and 15 July, 1982, in Parque Nacional de Santa Rosa, Guanacaste Province, Costa Rica. The area belongs to the premontane moist forest life zone (sensu Holdridge) and receives a mean annual rainfall of 2200 mm, which virtually all falls in the wet season months, May-November. Other physical and biotic details describing the area are given by Heithaus & Fleming (1978).

Experimental animals were captured with hand nets in day roosts or with mist nets either at roosts or at feeding patches within the first 30 minutes of evening flight activity; thus, hunger levels were approximately constant. Individual bats were identified to species, adult or juvenile age class, sex, and reproductive status. Forearm length and body mass were recorded and animals not previously colour-banded were marked individually by drops of coloured type-correction fluid on the crown of the head. Bats were released into the flight cage, one or two conspecifics per chamber, and allowed to feed as soon as possible after capture (usually within 1 hour). The outdoor flight cage was constructed of nylon mesh netting covering a wooden frame over a natural soil substrate and was divided into two 2 x 2 x 2 m chambers separated by mesh netting. Tin roofing sheets covered the mesh top of the cage to provide daytime shade and cover from rain.

All feeding experiments consisted of presentation of forty ripe bat-dispersed fruits which were suspended from the mesh ceiling by wire hooks. The forty fruits in each experiment consisted of twenty each of two plant species. Fruits were hung alternately by species in an 8 fruit x 5 fruit grid, each fruit being spaced 15 cm apart. Fruits were picked in late afternoon, placed in plastic bags by species, and kept on ice until the start of an experiment. Considerable care was taken to use only ripe, palatable fruit.

Initially, each bat released in the cage flew about exploring the cage for a period of 5-30 minutes before beginning to harvest and eat fruits. Animals that did not feed within 30 minutes of their introduction to the cage were set free. Bats were viewed under red or dim white light by an observer sitting inside each flight chamber. The observer recorded the time fruits were picked, the duration of handling by stopwatch, and the fruit species selected. That the observer and light appeared not to disrupt the bat's behaviour is evidenced by the fact that bats frequently roosted, ate fruits, and defecated directly over the observer's head.

Feeding experiments were terminated 90-240 minutes after the initiation of the first feeding bout depending on individual feeding rates and/or fruit availability on a given night. If a bat strongly preferred one fruit species, or ate half of the available fruit of one species, the grid was replenished with fruits during an experiment to restore the 20/20 ratio of fruit types.

RESULTS

Fruit handling times Handling times for the fruits of the eight plant species used are presented in Table 1.

Handling time was defined as time elapsed after a bat removed a fruit from its attachment site until all edible parts were consumed or inedible parts (e.g. skin) were discarded. Partially eaten and discarded fruits were not included in the analysis. We use 'fruit' to include all infructescences that were functionally one unit to the animals harvesting them (e.g. piper spikes). The results of the between-species comparisons of handling times of Piper amalago, Ficus ovalis, and Muntingia calabura fruits respectively were highly

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Fruit bat feeding/foraging variable. The null hypothesis that 'bat species do not differ in handling times of P. amalago' was rejected when the means in Table 1 were tested by one-way analysis of variance (ANOVA) with P

TABLE 1. Mean handling times (min) to consume fruits. Numbers are means and standard deviations. Brackets enclose mean mass (g) for fruits of plant species or bat species. Parentheses enclose sample sizes. Asterisks indicate fruit seldom if ever taken by wild bats in Parque

Santa Rosa Fruits of plant species

P. amalago F. ovalis M. calabura P. pseudoful. V. baccifera C. peltata F. morazaniana B. alicastrum Bat species [1-00] [0-94] [1.93] [1.52] [1-43] [6-30] [4-70] [4.12] C. subrufa [15-1] 0-45+0-12 0-76+0-34 0-67+0-31 0-96+0-43 1-18+0-22

(10) (18) (20) (07) (09) C. perspicillata [193] 0-79 +0-29 0-89+0-24 0-80+0-30 0-93 + 043 1.60 +088 1-40+ 1-16 . ?

(10) (18) (20) (13) (17) (22) G. soricina [10-3] 1-27+0-51 1-02+0-66 1-28+0-67 - 4-77+4-21

(07) (16) (18) (04) z A. toltecus [140] 11-52+3-87* 535 + 2-38 10-23 + 3-32 - 27-11+1.14 >

(06) (25) (21) (03) A. phaeotis [11-0] - 9-27?+439 11-71 +4-88 x

(05) (13) A.jamaicensis [45-5] 1-76+0-60* - 7-46+ 1.94 15-59+5-58 >

(07) (10) (09) S. lilium [15 9] 3-29+0-85 1-12+0-88 -- -

(05) (11) 0

TABLE 2. Multiple range test using the Student-Newman-Keuls procedure with ranges set for the 0-05 level and one-way ANOVA for interspecific comparison of mean food handling times (min) by bat species. Homogeneous subsets of bat species (whose highest and lowest means do not differ by more than the shortest significant range for a subset of that size) are denoted by brackets or parentheses. Values of F,

P, and degrees of freedom are for ANOVAS. Standard deviations and sample sizes are shown in Table 1

Piper amalago C. subrufa C.perspicillata G. soricina 1 A. toltecusi F=70-9, P

Fruit bat feeding/foraging

z *

8-

- ?I

60 120 180 Time (min)

FIG. 1. Cumulative food item feeding rates showing foraging bouts of individual G. soricina (GS) and C. perspicillata (CP). Intrerbouts are indicated by a 'Z'. Ficus ovalis and Muntingia calabura

are the fruits in these experiments.

When two or more conspecifics share a flight chamber, they usually cluster to sleep between semi-synchronized feeding bouts.

Carollia subrufa and C. perspicillata fed discontinuously (Figs 1, 2) in short bouts regularly spaced by longer interbout periods (Table 3). All twelve individuals of each Carollia species sampled exhibited stereotyped behavioural rhythms similar to the individuals in the figures. The two C. subrufa individuals plotted in Fig. 2 represent extremes in the variation observed in that species. Both Carollia species handled one or more fruits (0.6-2.5 g each) within a feeding bout, usually handling each fruit for less than a minute. Brief grooming of the fur and skin (about 30 s) took place after fruit consumption and before the search for another fruit. The search/selection component of feeding behaviour usually lasted only a few seconds. A fruit was often selected or rejected

TABLE 3. Feeding time budget parameters. Numbers in columns 3, 4, 5 are means and standard deviations. Sample sizes are in parentheses, column 3 and 4 sample sizes are identical. Foraging guilds are canopy frugivores (CF), groundstorey frugivores (GF), and nectar/pollen/insect omnivores (OM). A slash between

multiple guild designation indicates a species that switches guilds seasonally Foraging Fruits Feeding bout Interbout %0/ Time

Bat species guild per bout duration (min) duration (min) feeding C. subrufa GF 2-7?7-9 9 + 11 (43) 22+10 (39) 28 (7) C.perspicillata GF 1-9 ? 1 2 5+7 (54) 27+ 14 (44) 14 (8) G. soricina GF/OM 8.1 +7-9 38+45 (14) 18+7 (11) 73 (6) A. toltecus CF 114 + 8-7 89 + 55 (08) 21 + 5 (6) 88 (5) A. phaeotis CF 4-7+3-0 87+49 (07) 20+5 (4) 81 (3) A. jamaicensis CF > 14 (2) Continuous None observed 100 (2) S. lilium CF/GF > 18 (1) Continuous None observed 100 (1)

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F. J. BONACCORSO AND T. J. GUSH 32-

6 0 ^-

8 -''

60 120 180 240 Time (min)

FIG. 2. Cumulative food item feeding rates showing foraging bouts of individual A. toltecus (AT) and C. subrufa (CS). Interbouts are indicated by a 'Z'. Ficus ovalis and Piper amalago are the fruits

in these experiments.

after 'nosing' the fruit while hovering, and possibly represents an olfactory evaluation by the bat. Bats usually removed the pendant fruits from attachment hooks by mouth while hovering. In addition some individuals grasped a fruit with the hind feet to pull it free, and occasionally bats perched beside a fruit to eat it while it was still attached to the hook. Once picked, a fruit was taken in flight to a favoured spot or spots on the cage ceiling. These sites varied for each individual.

Seven of eleven Glossophaga soricina fed continuously throughout the 2-4 h experiments. The individuals that fed discontinuously in bouts had short interbout periods (mean = 18 min), and two of these fed continuously for more than 45 minutes. One typical adult male observed for 3 hours ate 27 fruits averaging about 1-5 g wet mass each. Given that about 25% of each fruit is discarded by G. soricina, the above bat consumed three times its own mass in 3 hours and continued to eat after our observations concluded!

The three species of Artibeus (n= 2-5) and Sturnira lilium (n= 1) fed continuously during the observations (Figs 2, 3). Feeding bouts were long, with many fruits handled successively per bout. Interbout roosting periods were infrequent and irregular in occurrence (Table 3), and some individuals took no interbout pauses in up to 4 hours of feeding.

The null hypothesis that 'bat species do not differ in food item feeding rate over a long portion of the night' was rejected when a one-way ANOVA (F ratio = 5-568; P


I - / O

60 I80 240 I I I 60 120 180 240

Time (min) FIG. 3. Cumulative food item feeding rates showing foraging bouts of individual S. lilium (SL) A. jamaicensis (AJ), and A. phaeotis (AP). Interbouts are indicated by a 'Z'. Brosimum alicastrum and Ficus morazaniana are the fruits available for the A. jamaicensis. Ficus ovalis and Muntingia

calabura are the fruits available to A. phaeotis and S. lilium.

Fruit species selectivity Of the twelve fruit-selectivity tests presented in Table 5, eight combinations showed no

selectivity (random feeding), three tests resulted in bats selectively feeding on the higher quality fruit, and one test resulted in Artibeus toltecus selectively feeding on the lower quality fruit. The percentage per g dry mass of protein, soluble carbohydrate, ash, and lipid in fruits we provided to experimental animals is as follows: Piper pseudo- fuligineum = P. amalago > Muntingia calabura > Ficus ovalis in each of the above nutrient types except that F. ovalis is ranked second in ash (Herbst 1983, 1986). Ficus ovalis ranks highest in fibre content but below the other three fruits in the above nutritional categories, and we designate it as a low-quality fruit compared with the other species tested. Large, bat-dispersed fig fruits from Panama similar to F. morazaniana and F. obtusifolia also are high in non-digestible fibre, moderate in soluble carbohydrate, and low in protein and lipid (Milton, Van Soest & Robertson 1980; Morrison 1980) compared to the pipers in Herbst's study. We tentatively assign F. morazaniana and F. obtusifolia to the low-quality fruit category for phyllostomid bats.

Groundstorey frugivores selected higher quality fruits over Ficus ovalis in three of the four bat-fruit pair combinations, and the fourth case (with Carollia subrufa) was barely below the 0-05 significance level. These same bat species showed no selectivity when

TABLE 4. Mean time taken to handle ten 1-2 g fruits. Homogeneous subsets of bat species as distinguished by a Student-Newman-Keuls multiple range test (P < 0-05)

are indicated by * or t Bat species x (min) S.D. n G. soricina* 78-2 23-4 11 C. subrufa* 97-3 31-1 12 A. toltecus*t 120-6 41-7 5 C. perspicillatat 133-7 41-9 12 A. phaeotist 160-7 62-0 3

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F. J. BONACCORSO AND T. J. GUSH TABLE 5. Pairwise selectivity of fruits by proportion of most nutritious fruit (first fruit in pair) out of the total fruits (number in parentheses) eaten in the sum of experiments (individual bats are pooled). Significant deviations from no selectivity are indicated by ** for P< 0.005 using a chi-square goodness-of-fit test, d.f. = 1. Plant species are P. psuedo-fuligineum (P. p.), P. amalago (P. a.), M. calabura

(M. c.), F. ovalis (F. o.) G. soricina C. subrufa C. perspicillata A. phaeotis A. toltecus S. lilium

P. p. vs. P. a. 065 (23) P.a. vs.M.c. 0-39 (18) 0-58 (66) 0.44 (16) P. a. vs. F. o. - 0.68** (63) 0.02** (45) M. c. vs. F. o. 0-86** (35) 0-57 (65) 0-77** (62) 0.70 (20) 0-61 (51) 0-50 (20)

Muntingia calabura fruits were paired against slightly better quality Piper amalago fruits, nor when nutritionally equivalent P. amalago and P. pseudo-fuligineum were paired. Though the three canopy frugivores showed no selectivity when high-quality M. calabura was paired against low-quality F. ovalis, they eat both fruits in the wild (Heithaus, Fleming & Opler 1975; Fleming et al. 1985). The only case of a canopy frugivore being tested on a high-quality fruit on which wild conspecifics normally do not forage versus a low-quality fruit (P. amalgo vs. F. ovalis) resulted in overwhelming selection of the low- quality but familiar dietary item (43 of 45 fruit choices) by two A. toltecus individuals. Invariably, the selectivity tests resulted in bats favouring fruits with which they were presumably familiar as free-roaming animals. When familiar with both fruits paired in the test, selectivity was shown only when fruits differed considerably in nutrient content.

Even bats that showed no selectivity between paired fruits in choice trials by the above criteria, actually may have fed selectively on one choice early in the experiment, and then may have reversed their selectivity later; or they may have fed non-randomly by frequently alternating food items on successive choices. This might have resulted from a need to obtain minimum requirements of two or more nutrients from different fruits. To evaluate this possibility, all food choice trials of individual bats were submitted to a runs test for dichotomized data (Sokal & Rohlf 1981) to determine whether the sequence of fruit choices was random or selective. Of the thirty-two trials in all paired fruit choice experiments, only three trials were found to show sequence selectivity by the runs test, where selectivity was not detected by the chi-square tests. One Carollia subrufa individual made fifteen switches (runs) in a sequence of twenty choices between Muntingia calabura and Piper amalago, more switches than expected by chance. Another C. subrufa chose Ficus ovalis in six of its first seven selections, but then selected thirteen consecutive M. calabura fruits, producing fewer switches than expected by chance. Finally, one Artibeus jamaicensis that ate ten F. morazaniana fruits and eight F. obtusifolia fruits made fewer switches (five) than expected by feeding exclusively on F. morazaniana early in the trial, then predominantly on F. obtusifolia later.

DISCUSSION

Canopy frugivore feeding behaviour and foraging strategy The canopy frugivores in this study characteristically feed continuously for long

periods and handled 20-80 fruits per night. Most of the nightly time budget ( > 80%) is spent feeding slowly (Table 3). Both captive (this study) and free-roaming (Heithaus, Fleming & Opler 1975; Bonaccorso 1979) bats select fruits that are low in nutrient content

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Fruit bat feeding/foraging compared either with other bat-dispersed fruits or with fruits eaten by obligate avian frugivores (Morrison 1980; Herbst 1983; Foster 1977; Foster & McDiarmid 1983). All stenodermines yet studied in detail specialize on fruits of large canopy trees (Gardner 1977; Morrison 1978a; Bonaccorso 1979; August 1981), particularly on mast-fruiting trees of the genus Ficus (Moraceae) which produce up to 500 000 fruits one or more times per year. These tree species tend to have clumped populations (Hubbell 1979), usually are present in very low densities (Fleming & Heithaus 1981), fruit asynchronously within a population (Morrison 1978a; Milton et al. 1982), and produce fruits for a relatively short number of days. Thus, canopy frugivores must be highly mobile to move among several feeding patches within a night (Morrison 1978a) and throughout the year.

The foraging strategy of canopy frugivores may be summarized as follows. Once a fruiting plant is located, a superabundant food source is assured for several days because all frugivorous animals combined usually do not reduce significantly the available edible fruits (e.g. on F. ovalis or F. insipida; F. J. Bonaccorso, unpublished data). Bats slowly handle and consume individual fruits with food being ingested at about the same rate that non-assimilated wastes are defecated (personal observation, this study) such that there is a continuous passage of nutrients through the gasto-intestinal tract. The dependence on low-quality food items ties up most of the nocturnal time budget with foraging and feeding. Reproductive males that defend tree hole roosts and harems may be particularly hard pressed to balance time-energy budgets because of conflicts between feeding and territorial defence (Morrison 1979; Morrison & Morrison 1981).

Groundstorey frugivore feeding behaviour and foraging strategy Groundstorey frugivores emerge from the day roost at the end of twilight to begin

foraging early relative to canopy frugivores (Bonaccorso 1979). Foraging is concentrated within variable-sized patches of selected shrubs (0. 1-3 0 m in height) and small trees (1-10 m in height) that produce 1-100 ripe fruits per plant per night of high-nutrient quality (Fleming 1982). These plants occur in moderate to high densities in their optimal habitats (Fleming & Heithaus 1981), but total ripe fruits per patch rarely approach 1000 per night. Although nightly availability per plant is low, fruit production is synchronized within populations and extends over weeks or months (Heithaus, Fleming & Opler 1975; Bonaccorso 1979; Fleming 1981) so that bats may return to the same resource patches for weeks before needing to locate a new food source. The ubiquitous, large, neotropical shrub genus Piper (Piperaceae) is a dietary staple of all members of the genus Carollia and typifies this fruiting pattern. Carolline bats thus forage on more spatio-temporally localized, predictable, but limited fruit resources than do stenodermine bats, and this is reflected in lower foraging distances traversed each night by carollines (Morrison 1978a; Heithaus & Fleming 1978; Fleming 1982).

As a night's feeding begins, groundstorey frugivores rapidly handle a succession of several fruits in a feeding bout (5-15 min) that ceases when gut capacity is reached (about 3-5 g of fruit pulp and seed). Bats remain inactive to digest and absorb nutrients at the night roost where feeding last occurred. Free-roaming radiotagged C. perspicillata have feeding bout and interbout rhythms similar to our captive bats (T. H. Fleming, personal communication). This suggests that the feeding bouts/interbouts we report here are not artefacts of captivity and represent a digestive bottleneck as has been observed in woodpigeons (Kenward & Sibly 1978). The gut is largely cleared of ballast (seeds and unassimilated pulp) within 20 min of interbout initiation (R. Lockwood, unpublished data; this study). The feeding cycle is repeated until daily nutrient requirements are

916


F. J. BONACCORSO AND T. J. GUSH satisfied or until sunrise. However, bats may have to switch food species and/or resource patches two or more times in a night if the preferred ripe fruits (e.g. pipers) and feeding patches become depleted (Fleming 1982; Fleming et al. 1985).

Actual foraging and feeding occupies only about one-sixth to one-third of the nightly time budget, and inactivity at night roosts accounted for much of the remainder in reproductively inactive bats. Territorial harem-defending males, however, return to the day roost during nearly every interbout to actively defend and patrol harem sites (Porter 1979; Williams 1986). Harem females and bachelor males rarely return to the day roost during interbouts and forage further from the day roost (1-3 km) than do harem- defending males (< I km) (T. H. Fleming, personal communication).

Feeding behaviour and foraging strategies of two generalists Unlike other stenodermine bats, Sturnira lilium is not a strict canopy frugivore

specialist. Twenty-one S. lilium fecal samples from Blancaneaux, Belize, contained seeds of eight plant species representing both canopy trees and small shrubs (F. J. Bonaccorso, unpublished data). The one captive Sturnira lilium individual we studied showed a diversified feeding behaviour. It handled high-quality fruits of limited abundance rapidly, but low-quality, superabundant fruits were handled slowly (cf. handling of Muntingia calabura vs. Ficus ovalis in Tables 1 and 2). This individual, run in only one feeding experiment, ate continuously and showed no selectivity between M. calabura and F. ovalis, and exhibited the fastest cumulative food item feeding rate of any bat studied. Sturnira lilium may be an extreme generalist among obligate frugivores. However, clarification of the foraging strategy of this species awaits more thorough study.

The one glossophagine species in our experiments, Glossophaga soricina, is an omnivorous generalist. Though more similar to groundstorey frugivores than to canopy frugivores, the foraging strategy of this species is intermediate to the more specialized frugivores, even during the early wet season when it is predominantly frugivorous. Fecal samples from free-roaming bats indicated that G. soricina usually did not select scarce piper fruits (Piper species fruits are eaten by captives when offered in artificially dense 'Piper food patches') and instead harvested somewhat less nutritious but more abundant fruits such as Muntingia calabura and Cecropia peltata (Heithaus, Fleming & Opler 1975). This bat species differed from the carollines in that it was slightly slower in handling fruits, it wasted a larger portion of each fruit, and its feeding rhythm was nearly continuous with irregularly occurring interbouts. It does appear to be able to compete with Carollia species for moderately abundant and high-quality fruits, which it preferred over Ficus species, but not for very low-density, high-quality Piper species fruits.

Foraging strategy comparisons Two distinct foraging strategies have evolved among phyllostomid bats that are

frugivores. Canopy frugivores specialize on superabundant and nutritionally low-quality fruits, are not affected by exploitative competition, and usually are not food limited. In the absence of bright moonlight, these bats spend most of the night engaged in nearly continuous feeding and foraging activities, and regularly make numerous visits to trees that attract large numbers of bats and bat predators. Canopy frugivores probably are subject to more severe predation pressure than groundstorey frugivores which forage among small plants, any one of which attracts only a few bats. Severe predation pressure also is suggested by the strong lunar phobia (Morrison 1978b) and mobbing behaviour in response to conspecific alarm calls (August 1979) of canopy frugivores.

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Groundstorey frugivores specialize on nutritionally high-quality fruits and handle fruits rapidly in quick, predictable timed feeding bouts in response to multi-species exploitative competition. These bats are so efficient at filling their stomachs with high- quality fruit, that most of the night is spent lightly sleeping at night roosts during digestive bottlenecks. Carollia subrufa and C. perspicillata are true foraging time minimizers sensu Schoener (1971), and this confers two adaptive advantages. First, inactive animals are less likely to attract predators than feeding animals. Second, reproductively active males are able to return to and defend harem sites from other males during feeding interbouts without comprising foraging time or greatly increasing energy budgets, though they cannot range as far as females and bachelor males from the day roost to forage.

ACKNOWLEDGMENTS

We thank the Servicio de Parques Nacionales, Costa Rica, for granting permission to do this work and the park personnel of Parque Nacional de Santa Rosa for logistical assistance. The staff of the Organization for Tropical Studies in San Jose provided logistical and clerical assistance. Financial support was provided by a Jessie Smith Noyes Grant (to T.J.G.) and NSF Grant DEB 81-04865 (to T. H. Fleming). T. H. Fleming and C. F. Williams assisted with the field work. J. Howard repeatedly saved our hard-found fruits from a pet magpie jay, and Flor de Canas helped us make it through the night. The manuscript was improved through the suggestions of J. A. Moreno, S. R. Humphrey, N. D. Johnson, and R. Thomas. This is Contribution No. 89 from the Program in Tropical Biology, Ecology, and Behavior of the University of Miami, Florida.

REFERENCES August, P. V. (1979). Distress calls in Artibeusjamaicensis: ecology and evolutionary implications. Vertebrate

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(Received 30 June 1986)

APPENDIX

Species of bats used in the feeding experiments Family Phyllostomidae

Subfamily Carollinae Carollia perspicillata (Linnaeus 1758) Carollia subrufa (Hahn 1905)

Subfamily Glossophaginae Glossophaga soricina (Pallas 1766)

Subfamily Stenoderminae Artibeus jamaicensis (Leach 1821) Artibeus phaeotis (Miller 1902) Artibeus toltecus (Saussure 1860) Sturnira lilium (E. Geoffroy St. Hillaire 1810)

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920 Fruit bat feeding/foraging

Species of plants used in the feeding experiments Family Elaeocarpaceae

Muntingia calabura [Swartz. (C. DC.)] Family Guttiferae

Vismia baccifera [Linnaeus (Tr. & P1.)] Family Moraceae

Brosimum alicastrum (Swartz.) Cecropia peltata (Linnaeus) Ficus morazaniana (Burger) Ficus ovalis [Liebm. (Miq)]

Family Piperaceae Piper amalago (Linnaeus) Piper pseudo-fuligineum (C. DC.)


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Issue Table of ContentsJournal of Animal Ecology, Vol. 56, No. 3 (Oct., 1987), pp. 723-1092+i-xiVolume Information [pp.i-xi]Front MatterSeasonal and Spatial Variation in Juvenile Survival of the Cabbage Butterly Pieris rapae: Evidence for Patchy Density-Dependence [pp.723-737]Ants, Parasitoids, and the Cabbage Butterfly Pieris rapae [pp.739-749]Kangaroos and Climate: An Analysis of Distribution [pp.751-761]Morphology, Echolocation and Resource Partitioning in Insectivorous Bats [pp.763-778]Group Living in the European Rabbit (Oryctolagus cuniculus): Mutual Benefit or Resource Localization? [pp.779-795]Adult Survivorship in Darwin's Ground Finch (Geospiza) Populations in a Variable Environment [pp.797-813]Lifetime Reproductive Success of Females of the Damselfly Coenagrion puella [pp.815-832]Random Patch Formation and Weak Competition: Coexistence in an Epiphytic Chironomid Community [pp.833-845]Breeding Seasons of North Scandinavian Starlings (Sturnus vulgaris): Constrained by Food or Time? [pp.847-855]Interactions Between Population Density and Maternal Characteristics Affecting Fecundity and Juvenile Survival in Red Deer [pp.857-871]Recent Changes in Host Usage by Cuckoos Cuculus canorus in Britain [pp.873-883]Stable Demographic Limit Cycles in Laboratory Populations of Tribolium castaneum [pp.885-906]Feeding Behaviour and Foraging Strategies of Captive Phyllostomid Fruit Bats: An Experimental Study [pp.907-920]Limitation and Regulation of Population Density in the Nuthatch Sitta europaea (Aves) Breeding in Natural Cavities [pp.921-937]Intraspecific Competition in Sticklebacks (Gasterosteidae: Pisces): Does Mother Nature Concur? [pp.939-947]Food Resource Partitioning Between Sympatric Populations of Brackishwater Sticklebacks [pp.949-967]Efficient Estimation of Age-Specific Survival Rates from Ring Recovery Data of Birds Ringed as Young, Augmented by Field Information [pp.969-987]The Allometry of Food Intake in Grazing Ruminants [pp.989-999]Movers and Stayers: Foraging Tactics of Young-of-the-Year Brook Charr, Salvelinus fontinalis [pp.1001-1013]Competition Between Larvae of the Field Cricket, Gryllus bimaculatus (Orthoptera: Gryllidae) and its Effects on Some Life-History Components of Fitness [pp.1015-1027]Factors Determining the Rate of Parasitism by a Parasitoid with a low Fecundity, Chrysis shanghaiensis (Hymenoptera: Chrysididae) [pp.1029-1042]Survival in Five Southern Albatrosses and its Relationship with Their Life History [pp.1043-1055]The Foraging Strategy of Diaeretiella rapae [pp.1057-1068]Territory Size and Population Limits in Mangrove Termites [pp.1069-1081]Reviewsuntitled [p.1083]untitled [pp.1083-1084]untitled [pp.1084-1085]untitled [pp.1085-1086]untitled [pp.1086-1087]untitled [p.1087]untitled [p.1087]untitled [pp.1087-1088]untitled [p.1088]untitled [p.1088]untitled [pp.1089-1090]Short Notices [pp.1090-1092]

Back Matter [pp.iv-iv]

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