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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:
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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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'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
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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
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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
-
Fruit bat feeding/foraging
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
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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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Fruit bat feeding/foraging
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.
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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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Article
Contentsp.907p.908p.909p.910p.911p.912p.913p.914p.915p.916p.917p.918p.919p.920
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]