An Experimental Analysis of the Food Location Behavior of Frugivorous Bats

Author(s): Theodore H. Fleming, E. Raymond Heithaus and William B. Sawyer

Source: Ecology, Vol. 58, No. 3 (Late Spring, 1977), pp. 619-627
Published by: Ecological Society of America
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Ecology (1977) 58: pp. 619-627

AN EXPERIMENTAL ANALYSIS OF THE

FOOD LOCATION BEHAVIOR OF FRUGIVOROUS BATS'

THEODORE H. FLEMING
Department of Biology, University of Missouri, St. Louis, Missouri 63121 USA

E. RAYMOND HEITHAUS
Department of Biological Sciences, Northwestern University, Evanston, Illinois 60201 USA
AND
B. SAWYER
WILLIAM
Department of Anthropology, Washington University, St. Louis, Missouri 63130 USA

Abstract. Models of optimal foraging often separate the time and energy expended in getting to a
feeding area (commuting costs) from the time and energy expended in searching for food (search costs)
in animals that are "pure searchers." We predict that under certain circumstances (e.g., a relatively
uniform resource distribution) searching and commuting behavior will be synchronous, whereas under
other circumstances (e.g., a relatively patchy resource distribution) these two behaviors will be
temporally separated. We have tested these predictions by studying the foraging and food location
behavior of several species of Costa Rican frugivorous bats using mist-netting programs, radio-
telemetry, and fruit relocation experiments. Concurrent observations were made on the phenology and
distribution patterns of the six fruit species used in the relocation experiments. The mist-netting
program allowed us to determine the food habits of the common frugivorous bats in our study area and
to identify the major chiropteran dispersal agents of the six fruit species. The radio-tracking program
provided detailed information on the foraging behavior of one of the most important seed dispersal
agents, Carollia perspicillata, whose individuals commute up to 2.7 km from a central day roost before
beginning to feed.
Results of the fruit relocation experiments, in which ripe fruits of the six species were individually
placed on "fruit poles" located either close to or at a considerable distance (>0.5 km) away from con-
specific plants in areas known to be used by bats, indicated the following: (1) fruits of two species of
Piper, which are highly preferred by Carollia and which occur in low nightly densities for extended
periods of time, had as high (-.90) a probability of being found away from nonspecific plants as when
they were near conspecifics; (2) fruits of two species of Ficus and Muntingia calabura, which are very
patchily distributed in time and/or space, had a significantly higher probability (.30-.50 vs. .02-.12) of
being found near rather than away from conspecifics; and (3) when placed on poles with Piper fruits,
fruits of Ficus ovalis, Chlorophora tinctoria, and Muntingia calabura had a significantly higher proba-
bility (.40-.60 vs. .08-.13) of being found than when placed in similar areas without Piper fruits. These
results indicate that certain bats (e.g., Carollia perspicillata and Glossophaga soricina) are constantly
"on the alert" for ripe Piper fruits while commuting, whereas bats that eat Ficus, Chlorophora, or
Muntingia fruits (e.g., G. soricina orArtibeusjamaicensis) are not constantly "on the alert" for these
fruits while commuting. Bats feeding on Piper probably search and commute simultaneously, whereas
those feeding on Ficus or Muntingia separate commuting and searching behavior. The food location
behavior of frugivorous bats appears to be highly responsive to differences in the spatiotemporal
distribution patterns of their food resources.
Key words: Optimal foraging; frugivorous bats; Costa Rica.

INTRODUCTION costs and benefits (see Hamilton and Watt 1970,

Schoener 1971), then the spatial and temporal distribu-
The research described in this paper is directed at
tion of food should influence food location behavior.
the general problem of how frugivorous bats search for
When food is distributed in relatively uncommon, iso-
and locate their food. We specifically asked the ques-
lated patches there should be little "return" for
tion: How sensitive is the food location behavior of
searching for food between known patches. Therefore,
frugivorous bats to the spatiotemporal distributions of
a forager should first commute and then search only
their food resources? Since many frugivorous bats
after arriving at a feeding area. When food is distrib-
commute between a day roost in which they rest and
uted more evenly, the added potential gain from
sleep and their nocturnal feeding areas, the question
searching should eventually promote combined com-
arises as to whether they actively search for food while
muting and searching. If these predictions are not sup-
they commute or whether they temporally separate
ported, then additional factors, such as social interac-
food location and commuting behaviors.
tions, must be included in explanations of patterns of
If foraging is responsive to a balance of energetic
foraging.
1 Manuscriptreceived 26 April 1976;accepted 4 February Some background information on fruit-eating bats is
1977. necessary before we indicate how we tested these pre-

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620 THEODORE H. FLEMING ET AL.
dictions. Several characteristics of this group are im-
portant to studies of foraging. First, using Schoener's
(1969) terminology, frugivorous bats are "pure search-
ers." Once food is located, it need not be pursued or
subdued. This reduces both magnitude of the "food
handling" costs and variation in handling costs for dif-
ferent food types and leaves site location and commut-
ing and searching costs as the primary energetic con-
siderations for foraging in frugivorous bats. Second,
they feed on noncryptic, particulate foods (fruits)
whose density and dispersion can be measured. Third,
the food habits of these animals can be assessed using
nondestructive techniques (Heithaus et al. 1975). Fi-
nally, many species are relatively sedentary and long-
lived (Fleming et al. 1972, Wilson and Tyson 1970), so
their foraging behavior should reflect conditions in an
area small enough to study thoroughly.
Information concerning the following four param-
eters is necessary to test our predictions about the com-
bination of commuting and searching behavior: (1) the
identity of the preferred fruits of the bat species in one
area; (2) the density and dispersion patterns of these
fruits; (3) whether or not bat species in the study area
commute to regular feeding areas; and (4) whether or
not any bat species commute and search simulta-
neously. Determination of the first two parameters is
straightforward. Our approach to studying parameter
(3) is to follow bat foraging by means of radio-
telemetry. Using this technique we see whether bats
repeatedly use the same resource patch, a behavior
that requires "commuting." To see whether bats
search while commuting (parameter 4), we move fruits
away from fruiting plants and measure their probabil-
ity of being located and eaten by bats. We predict that
relocated fruits that normally are distributed in low,
rather uniform densities should be found more readily
than relocated fruits that usually occur in isolated
clumps.
STUDY AREA AND METHODS
This study was conducted at Parque Nacional Santa
Rosa, 28 km NW of Liberia, Guanacaste Province,
Costa Rica, in the Premontane Moist Forest zone of
Holdridge (1967). Rainfall at Santa Rosa, which aver-
ages 2,200 mm annually, is seasonal with a severe
6-mo dry season occurring between mid-November
and mid-May. Parque Nacional Santa Rosa consists of
a mosaic of habitats, including various seral stages of
dry forest, evergreen forest in moist ravines, fire-
maintained savannas, and abandoned pastures. Since
Santa Rosa was an important cattle ranch for 300 yr
before becoming a national park in 1971, habitat dis-
turbance is of long-standing occurrence (G. Canessa,
personal communication).
Santa Rosa contains many of the same species of
bats and their fruit and flower resources as Finca La
Pacificia, our previous bat-plant study site (Fleming et
al. 1972, Heithaus et al. 1975) which is located 70 km
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Ecology, Vol. 58, No. 3
SE. Mist-netting during July and August 1974 and 1975
resulted in the capture of 21 species of bats, including
13 frugivorous species of the family Phyllostomatidae.
At least 11 fruit resources are available in July and
August, including four produced by shrubs (Piper
amalago, Piper pseudofuligineum, Piper jacquemon-
tianum, and Solanum hazeni) and seven produced by
trees (Cecropia peltata, Chlorophora tinctoria, Ficus
cotinifolia, Ficus ovalis, Ficus obtusifolia, Ficus sp.,
and Muntingia calabura); an additional four species of
unidentified seeds have been found in bat fecal sam-
ples. One flower resource, Crescentia alata, is avail-
able in July and August.
Mist-netting and radio-tracking programs were con-
ducted simultaneously with the fruit relocation exper-
iments that form the core of this study. Ten 6- or 12-m
Japanese mist nets were set at ground level in several
of the experimental areas to determine the composi-
tion of the bat population in each area and the food
habits of the frugivorous bats. Bats were examined
and many were banded before being released. Fecal
samples containing seeds were collected and placed in
numbered glassine envelopes for later identification.
We captured 1,599 bats and collected 537 fecal sam-
ples. Radio-tracking techniques will be reported
elsewhere.
Fruit detection away from resource patches was
tested by placing fruits on "fruit poles" in or away
from conspecific resource patches. Fruits were placed
on 1-cm, upward pointing wire spikes spaced at 5- to
10-cm intervals along a small branch (1 cm in diame-
ter x 30 cm long) attached to the top of 148-cm-long
poles. Experiments typically utilized six poles bearing
a total of 18 or 36 fruits and placed at 5- to 6-m inter-
vals along mist net lanes, narrow roads, or in natural
clearings. Fruits were usually collected in the after-
noon of the experiment. Most experiments utilized
ripe fruits, which were kept in plastic bags until being
placed on the poles. In the case of Chlorophora, fresh
fruits were sometimes taken from the ground where
they had been dropped by monkeys, other arboreal
mammals, or birds. The poles were usually set up
15-45 min before sunset. On several occasions the
poles were checked at various times during the night.
The presence or absence of fruits was recorded within
1 h after sunrise the next morning. Since it is highly
unlikely that mammals such as opossums (Didelphis
virginiana) or frugivorous birds such as trogons or par-
rots could have removed fruits from the poles without
knocking the poles down, we feel confident that the
disappearance of fruits from upright poles was caused
by bats. Fruits on fallen poles were not counted as
being "exposed" to bats.
Two variations on the basic experimental scheme
were employed with fruits of Ficus and Chlorophora.
For Ficus cotinifolia and F. ovalis, we placed poles in
two or four transects, 10 poles spaced at 5-m intervals
per transect, running 30-50 m from the base of a fruit-
Late Spring 1977 FOOD LOCATION BEHAVIOR IN FRUGIVOROUS BATS 621

area under the canopy of a fruiting Ficus tree. Flyways

were obvious clearings such as trails and narrow roads
along which bats were observed to fly; in these areas
care was taken not to place fruit poles near (within 50
m) a potential bat resource. Nonresource areas or
patches refer to either (1) natural forest clearings away
from bat resources or (2) forest clearings that contain
nonconspecific bat resources. For example, Ficus
fruits placed on poles in or near a Piper patch consti-
tuted an experiment utilizing a "nonresource" patch
A from the viewpoint of Ficus. On any given night poles
containing a single fruit species were placed in two
different areas, a control area (=resource patch) and
an experimental area (=flyway or nonresource patch).
Whenever possible, experiments were replicated at
least twice (see Table 6).
The phenology and density and dispersion patterns
of the six species of fruit used in the relocation exper-
>01 tK_*e* n
iments were studied in detail. Numbers of flowers
and/or ripe fruits on labeled census trees were
counted or estimated at weekly or biweekly intervals.
H.A Densities of both Piper species in areas B and C were
estimated using the point-quarter method (Cottam et
al. 1953). Actual densities and dispersion patterns of
.-Fol each of the species were obtained by mapping the loca-
Fc
tions of trees and shrubs on an 800- x 100-m area (8
ha) gridded at 20-m intervals (Fig. 1). This area, which
represents one third of a 24-ha grid constructed by Dr.
FIG. 1. Location of the fruit pole experiments. A Carollia
Stephen Hubbell and several University of Iowa stu-
perspicillata and Glossophaga soricina roost is designated R. dents, includes relatively mature dry tropical forest as
Forested areas are stippled. The dashed lines indicate loca- well as younger forest.
tion of the 8-ha grid.
RESULTS

Relative abundance and species composition

ing tree. One 20-pole experiment was run under a F.
ovals tree and three 40-pole experiments were run of bats in the experimental areas
under a F. cotinifolia tree. For Chlorophora tinctoria, We have used the rate of capture of bats, expressed
several experiments were run using a vertical transect as number of bats captured per net-hour, as an index
in which three 1.2-m samplings each containing 10 of the relative abundance in several of the areas where
wire spikes placed at 7.5-cm intervals were firmly at- we placed fruit poles (Table 1). There were differences
tached to a rope line thrown over a fruiting branch 6 to between areas regarding rates of capture: rates were
8 m above the ground. The horizontal bars were higher under two isolated Ficus trees. Our overall
spaced at 1.5-m intervals along the rope below the conclusion from these results is that there is increased
branch. Fruits were placed on the bars and raised into bat activity around fruiting fig trees, but similar num-
position just before sunset and were scored just after bers of bats were flying along or in the flyways and
sunrise to avoid possible loss of fruits to monkeys. Piper resource patches.
In addition to single species experiments, several The species composition of frugivorous bats differed
mixed species experiments were run. In these two significantly among areas. The two most commonly-
fruits of each of three species (e.g., Piper netted bats in most areas were Carollia perspicillata
pseudofuligineum, Chlorophora tinctoria, and Mun- (most common in areas A, B, and C) and Artibeus
tingia calabura) were placed alternately on the same jamaicensis (most common in area D and at Ficus
pole. cotinifolia); Glossophaga soricina was the most com-
Experiments were conducted in a total of 14 differ- mon bat at F. ovalis (Table 2). Chi-square analysis in-
ent locations, including resource patches, resource- dicated no difference in species composition for 2 yr in
free bat flyways, and "nonresource" patches (see Fig. areas A and C. Artibeus jamaicensis was significantly
1 for locations of these areas). Resource patches refer less common in area B in 1975 than in 1974
to areas where ripe conspecific fruits were available. (.025 > P > .01). Bat composition in the two Piper
For example, a Piper resource patch contained many areas (B and C) differed significantly in both years,
fruiting Piper plants; a Ficus resource patch was the with area B containing a higher proportion of "other"

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622 THEODORE H. FLEMING ET AL. Ecology, Vol. 58, No. 3

TABLE 1. Rate of capture of bats at Santa Rosa in July and August of 1974-75

No. of bats per net-hour

No. of times Total no. of
Netting area Type of netting site sampled net-hoursa x SD
A Flyway and roost 7 289 1.74 1.07
B Piper resource patch 6 210 1.01 0.48
C Piper resource patch 5 183 1.35 0.56
D Flyway 2 80 1.41
Ficus ovalis Resource patch 2 20 3.65
Ficus cotinifolia Resource patch 2 31 2.47
a One net-hour = one mist net opened for 1 h.

species and a lower proportion of G. soricina. Two
relatively close netting sites, C (a Piper patch) and D
(a flyway) (Fig. 1), were dominated by different species
(Table 2). If these results accurately reflect the com-
position of bats passing through and utilizing the dif-
ferent areas, then fruits placed on poles in these areas
were being exposed to different combinations of bat
species in different relative proportions.
Food habits of the bats
Body weights and food habits, as determined by the
analysis of their fecal samples, of the six most
commonly-netted frugivorous bats are presented in
Table 3. Four of the six species are relatively small
(<20 g); two species are medium- to large-sized
compared to other phyllostomatid bats. Of these
species, Carollia perspicillata has the most diverse
diet but tends to concentrate on Piper fruits. Glos-
sophaga soricina and Sturnira lilium also eat Piper
fruits and have relatively broad diets. Species of Ar-
tibeus have narrower diets and tend to concentrate on
fruits of the Moraceae (Ficus, Chlorophora, and Ce-
cropia).
In addition to knowing the food habits of the bats, it
is also important to know the major dispersal agents of
the fruits we were studying (Table 4). The two Piper
species are dispersed by only three or four species
with Carollia perspicillata being the major dispersal
agent. Three species, Ficus cotinifolia, F. ovalis
(whose seeds are indistinguishable), and Chlorophora
tinctoria, are more evenly represented in the diets of
several species of bats. Muntingia calabura is dispersed
primarily by Glossophaga soricina. Species other than
Piper are also dispersed by a variety of other verte-
brates.
Plant density, dispersion, phenology, and
fruit characteristics
Six species of fruit were placed on fruit poles. As
detailed below, these species differed considerably re-
garding their density, dispersion, phenology, and fruit
characteristics. Because of these differences, we ini-
tially predicted that the bats would use different com-
binations of searching and commuting behaviors to lo-
cate these fruits.
Piper amalgo L.-This 1- to 3-m shrub attains its
greatest density in moist portions of deciduous forest.
Representative densities in areas B and C, respec-
tively, were 398 and 222 plants per ha (also see Table
5). It also occurs at lower densities along forest trails,
in clearings, and in evergreen forest. Its dispersion
pattern was significantly clumped on the 8-ha grid (Ta-
ble 5). Phenological observations indicate that plants
flower and fruit cyclically during the wet season. Ripe
fruits first appear =1 mo after the beginning of heavy
rains (mid-May to early June), and the first fruit cycle
lasts =1 mo, ending in early August in 1974 but lasting
until late August in 1975. On any given night during
this cycle, only =z5% of the fruits are ripe. The mean
number of ripe fruits (actually, infructescenses) on 100
randomly-sampled plants in area C on 17 July 1974 was
0.27 (SD = 0.67); upon extrapolation the density is
60.1 ripe fruits per ha- night. The probability that all of
these fruits will be located and removed by bats on the

TABLE 2. Bat species composition in the netting areas in July and August 1974-75. Species abbreviations as in Table 3.
Number of other species in parentheses

No. of Proportion of total bats, by species

Netting area times Total no.
and year sampled of bats CP GS SL AJ Others
A, 1974-75 7 363 .570 .127 .022 .135 .146 (6)
B, 1974 4 151 .431 .126 0 .278 .165 (5)
B, 1975 2 54 .630 .130 .019 .093 .128 (2)
C, 1974-75 5 212 .401 .198 .066 .236 .099 (5)
D, 1974 2 110 .200 .082 .046 .464 .208 (5)
Ficus ovalis, 1974 1 14 0 1.000 0 0 0
F. ovalis, 1975 1 61 .115 .426 .082 .066 .310 (4)
F. cotinifolia, 1974 2 76 .026 .066 .026 .605 .277 (6)

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Late Spring 1977 FOOD LOCATION BEHAVIOR IN FRUGIVOROUS BATS 623

TABLE 3. Weight and food habits of six species of frugivorous Costa Rican bats. Data are from July and August 1974-75.
See Table 5 for plant names. H', the Shannon-Wiener information-theoretic index, is calculated as H' = -E pi In pi

Proportion of fecal samples containing seeds of: Food

Aver- Fecal niche
age samples FO + breadth
Species wt (g) (n) PA PP pja FC FSppb CT CPC MC SHd H'
Carollia perspicillata
(Cp)e 19 269 .320 .279 .033 0 .004 .112 .138 .026 .089 1.683
Glossophaga soricina
(GS) 11 85 .212 .224 0 .141 0 0 .212 .212 0 1.597
Sturnira lilium
(SL) 15 56 .054 .054 .179 0 0 .125 .357 0 .232 1.588
Artibeus jamaicensis
(AJ) 46 97 0 0 0 .072 .216 .289 .423 0 0 1.244
A. lituratus (AL) 60 19 0 .053 0 0 .053 .474 .421 0 0 1.028
A. phaeotis (AP) 12 9 0 0 0 .333 0 .333 .333 0 0 1.099
a Piper jacquemontianum.
b
Large-seeded Ficus spp.
c Cecropia peltata.
d Solanum hazeni.
e Abbreviations used in other tables.

first night they are ripe is nearly 1.0 (T. H. Fleming
and E. R. Heithaus, personal observation). There
are at least two fruit cycles in the reproductive season
of this species. Infructescences of P. amalgo weigh
1.6 g, are about 48 mm long and 4 mm wide, and are
exerted vertically away from the foliage of the shrubs.
They detach easily from branches only when ripe, at
which time they are soft to the touch and differ from
unripe fruits in color (dark green vs. lighter green) and
probably odor. Bats can remove ripe fruits while in
flight rather than after first landing on a branch.
Piper pseudofuligineum C. DC.-This 1- to 3-m
shrub is found in a variety of successional and edaphic
habitats but never is as abundant as other Piper
species in the same habitats. It cooccurs with Piper
marginatum in early successional forest or large forest
clearings, with P. amalago in moist deciduous forest,
and with P. jacquemontianum in evergreen forest at
Santa Rosa. Its density in areas B and C was about 19
and 50 plants per ha, respectively, and its dispersion
was significantly clumped on the grid (Table 5). Like
P. amalago, P. pseudofuligineum flowers and fruits
cyclically in the wet season. In any given habitat, its
ripe fruits (infructescenses) are available later in the
season than those of P. amalago. These two species
have temporally displaced fruit (and flower) cycles. In
1974 the mean number of ripe fruits per plant night in
area C was 2.46, which extrapolates to a density of
123.2 ripe fruits per ha night. Most of these fruits will
also disappear on the first night they are ripe; bats
appear to be their sole dispersal agents. Infructes-
cences of P. pseudofuligineum weigh 2.3 g, are -70
mm long and 3 mm wide, and are similarly oriented
and share other attachment characteristics with their
congener. When ripe, fruits are soft and differ from
unripe fruit in color (mustard yellow vs. drab tan) and
probably odor.
Ficus cotinifolia H. B. K. and F. ovalis (Liebm.)
Miq.-Because they are difficult to distinguish vegeta-
tively and have similar-sized fruits and similar seed
morphologies, we have combined these species under
a single account. These large trees occur at low densi-
ties (<1 per ha) in forest and as scattered trees in
pastures and around human habitations; they were
randomly distributed on the grid (52 X; Table 5). Both
species probably fruit asynchronously throughout the

TABLE 4. Bat dispersal agents of six species of Costa Rican fruits. Data are from July and August 1974-75

Plant
dispersal
Fecal Proportion of fecal samples from: niche
Plant samples breadth
species (n) CP GS SL AJ AL AP CVa H'
PA 107 .804 .168 .028 0 0 0 0 0.576
PP 98 .765 .194 .031 0 .010 0 0 0.676
FO + FC 25 0 .480 0 .280 0 .120 .120 1.218
CT 77 .481 0 .091 .364 .117 .039 0 1.330
MC 25 .280 .720 0 0 0 0 0 0.593
a Chiroderma villosum.

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624 THEODORE H. FLEMING ET AL.
TABLE 5. Density and dispersion patterns of several species of bat-dispersed plants. Data are from an 8-ha grid staked
at 20-m intervals. Number of quadrats analyzed = 205
Density/quadrat
Species and family x Density/ha
Piper amalago
(PA)b (Piperaceae) 7.3 184.8
Piper pseudofuligineum
(PP) (Piperaceae) 0.7 2.0
Ficus cotinifolia and
F. ovalis (FC, FO)
(Moraceae) 0.03 0.02
Chlorophora tinctoria
(CT) (Moraceae) 0.4 0.6
(sexes combined)
Muntingia calabura
(MC) (Elaeocarpaceae) 0.08 0.2
a Is = 1.0 for a random distribution. Values significantly greater or less than 1.0 indicate clumped or uniform distribu-
tions, respectively.
b Abbreviations used in other tables.
year, further lowering their "economic" densities; in-
dividuals fruit more than once a year. Fruit crops can
be enormous in size (up to an estimated 20,000 per tree
in a fully isolated situation) and the crop is removed
relatively rapidly (in less than 3 wk) by birds, bats, and
arboreal mammals. The fruits (actually, infructes-
censes) of these species are small ("" 1 g), oval (diame-
ter = 11 mm), red in color when ripe, and are tightly
attached to branches (F. ovalis) or slightly stalked (F.
cotinifola) amid foliage. Fruits detach easily only
when ripe. Bats probably have to land on a branch or
foliage before removing a fruit.
Chlorophora tinctoria (L.) Gaud.-This dioecious
tree species occurs at moderate densities (several in-
dividuals [sexes combined] per ha) in forest and as a
planted species around human habitations; its disper-
sion pattern was clumped on the grid (Table 5). Its
reproductive season is restricted to the wet season
(Heithaus et al. 1975). Ripe fruits (infructescenses)
first appear in middle to late July. Individuals can have
up to several thousand fruits in a single crop that lasts
2-4 wk. Fruits are eaten by a variety of birds, bats, and
arboreal mammals. They are green and berry-like (di-
ameter = 13 mm), weigh 3.2 g, exude a milky latex
when ripe, and resemble Ficus fruits in method of at-
tachment to branches. Bats probably have to land on
branches or foliage to remove fruits.
Muntingia calabura L.-This small tree grows in
clumps of several individuals, usually in disturbed
areas. Unlike Ficus and Chlorophora it is not a mature
forest species. It occurred in low density and was
strongly clumped on the grid (Table 5). The phenology
of M. calabura more closely resembles that of Piper
than either Ficus or Chlorophora in that individual
trees produce relatively few (up to 20) ripe fruits per
day for extended periods of time. At La Pacificia, this
species fruits and flowers year-round (Heithaus et al.
1975). The fruits, whose complete list of dispersal
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Ecology, Vol. 58, No. 3
Morisita's
index
I~a F-value P
181.8 4.5 25.9 <.005
19.9 3.5 2.9 <.005
0.6 ---- ---- ----
9.5 2.6 1.6 <.005
1.9 24.8 2.7 <.005
agents is unknown, are relatively small (1.4 g), ovoid
(greatest width = 10 mm), red in color and sweet-
smelling when ripe, and hang below the foliage from
25-mm flexible stems from which they are plucked by
flying bats.
In summary these six plant species fall into three
classes regarding their density, dispersion and phenol-
ogy. Species in the first class, which includes both
Piper species, usually occur in patches of several to
many individuals in a variety of different habitats.
Patch density can be quite high under suitable edaphic
conditions, but many plants are found outside these
patches. Their phenology includes the production of
low numbers of ripe fruits each night for several
weeks. From the viewpoint of a frugivorous bat, there-
fore, nightly fruit density in these species tends to be
low and moderately patchy in distribution. We predict
that bats will search for these species while commut-
ing. Species in the second class, which includes both
Ficus species and Chlorophora tinctoria, occur as
widely-spaced individuals bearing large but short-lived
fruit crops. We predict that bats will not search for
these fruits while commuting. The third class includes
Muntingia calabura, a species with a highly-clumped
distribution but a low, relatively constant availability
of fruit year-round. We predict that bats will not
search for these fruits while commuting.
Commuting behavior of bats
Using radiotelemetry we have determined the
foraging paths of 24 individuals of Carollia perspicil-
lata for periods as long as 3 wk (E. R. Heithaus and T.
H. Fleming, personal observation). Each individual
consistently commuted from a day roost to the same
set of foraging areas on successive nights. The average
distance from day roost to feeding areas was 1.0 km
and the longest commuting distance was 2.7 km. The
average flight speeds from roost to foraging area var-
Late Spring 1977 FOOD LOCATION BEHAVIOR IN FRUGIVOROUS BATS 625

TABLE 6. Summary of the fruit pole experiments. Unless indicated, all experiments utilized ripe fruits

Experi- No. of fruits

Fruit ments Removed
species Location or condition Sites utilized (n) Exposed Removed (%)
PA 1) Resource areas B, C 6 111 73 65.8
2) Flyways A, D, E, J 10 148 142 95.9
3) Other areas F, G, H 3 54 45 83.3
4) Area B vs. 3 56 24 43.6
Area C 55 49 87.5
5) Ripe vs. B, C 2 76 47 61.8
Unripe 35 1 2.9
6) Single vs. B, C 2 19 11 57.9
Multiple 18 7 38.9
PP 1) Single vs. B, C 2 21 20 95.4
Multiple 18 17 94.4
2) Resource areas B, C 4 59 55 93.2
3) Flyways or other areas A, I 2 20 19 95.0
FO & FC 1) Resource areas FOI, F02 8 216 87 40.3
2) Flyways or other areas A, B, C, I, J 14 194 19 9.8
3) Under fruiting tree vs. FOI, FC 4 144 33 22.9
away from tree in transect 266 32 12.0
4) In presence of Piper A, J 2 15 6 40.0
pseudofuligineum
5) In presence of Piper A, J 2 36 1 2.8
(llnlag(o
CT 1) Resource areas C, I 7 190 6 3.2
2) Flyways or other areas A, B, C 5 30 4 13.3
3) In presence of Piper A, B, C, 1 4 40 24 60.0
pseudofuligineum
MC 1) Resource area L, K 3 42 13 31.0
2) Flyway A 2 32 2 6.3
3) In presence of Piper A, C, 1 4 40 19 47.5
pseudofuligineum

ied, even for the same bat on different nights, so it cent ripe fruits removed in the two Piper patches,
appears commuting flights for Carollia perspicillata areas B (44%) and C (88%), in both 1974 and 1975,
are not necessarily direct and rapid. Observations perhaps because Glossophaga soricina, the second
made by Morrison (1975) and our data (personal ob- most important dispersal agent of P. amalago, was
servation) suggest that Artibeus jamaicensis does not less common in B than in C (Table 2). The relatively
roost in its feeding tree(s) but flies some distance, usu-
low removal percentage in area B makes the resource
ally greater than 0.5 km, to a feeding area. No radio- patch vs. flyway-nonresource patch x2 compari-
tracking data are available for other species, but Glos- son significant (P < .01); dropping area B from this
sophaga soricina roosts colonially and hence is a ref- comparison makes the differences nonsignificant
uging species that must also commute to its feeding (P > .25). A significant difference also existed in re-
areas. It is likely that most, if not all, of the frugivo-
moval percentages between flyways and "other
rous species in our area must commute between day areas" ( = nonresource patches) (.025 > P > .01).
roosts and feeding areas. These differences likely result from a higher density of
bats in the flyways than in the nonresource areas.
Results of the fruit relocation experiments
We performed additional experiments to see
Results of the fruit pole experiments are sum- whether bats could distinguish between ripe and un-
marized in Table 6. Below we discuss the results for ripe fruits and whether three fruits on a pole stood a
each species separately. better chance of being found than single fruits. Results
Piper amalago.-The major hypothesis being tested of the two experiments in which three unripe fruits
in these experiments was that P. amalago fruits on were alternated with three ripe fruits on each of six
poles away from resource patches had as high a prob- poles (Table 6) indicated that bats readily discriminate
ability of being located as those on poles in the between ripe and unripe fruits: only 3% of the unripe
resource patches. Results of 19 experiments are con- (in our judgment) fruits were taken compared to 62%
sistent with this hypothesis (Table 6). There was a sig- of the ripe fruits. A higher proportion of the single
nificant difference (X2 = 21.8, P < .005) in the per- fruits were taken (58% vs. 39%o)but the difference was

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626 THEODORE H. FLEMING ET AL.
not significant when tested by chi-square. A single
fruit on a pole has as high a probability of being located
and removed as do several fruits on a pole. Tagging
solitary vs. several ripe fruits on shrubs yields the
same results: bats locate both kinds of fruits with
equally high probability.
P. pseudofuligineum.-As with P. amalago we
wanted to know whether single fruits had the same
probability of being found as several fruits on a pole;
they do (Table 6). Results of the resource patch vs.
flyway and other area comparison again support the
major hypothesis. As least 93% of the fruits placed in
either kind of area were taken by bats. To judge from
the bats' food habits (Table 3), Carollia perspicillata
and Glossophaga soricina are responsible for remov-
ing the fruits of P. pseudofuligineum, as well as those
of P. amalago.
Ficus ovalis and F. cotinifolia.-The bulk of our
data come from F. ovalis. Results of the transect ex-
periments were similar in both species and are herein
combined. We predicted that fruit of these species
placed on poles under fruiting trees would have a higher
probability of being taken than those placed on poles
in flyways or other nonresource areas. Results of 22
experiments (Table 6) are consistent with this expecta-
tion: 40% of "resource area" fruits were taken com-
pared to only 10% of the "nonresource area" fruits;
this difference is statistically significant (P < .005).
Also significant (P < .01) was the difference between
removal percentages of fruits located under the tree
(23%) or away from the canopy in transects (12%).
Bats appear to be most "sensitive" to Ficus fruits only
in the immediate vicinity of the fruiting tree. Results of
two experiments in which Piper pseudofuligineum and
Muntingia calabura fruits were alternated with fruits
of F. ovalis (in nonresource areas) suggest that bat
"sensitivity" to Ficus can be increased by the pres-
ence of Piper (or Muntingia). Removal percentages
(40%) in the mixed species experiments were as high
as when fruits were placed under the fruiting tree and
were significantly higher (P < .01) than control fruits
placed in nonresource areas in the absence of Piper
(Table 6). In the presence of just Piper amalago, how-
ever, only one of 36 fruits was taken. The combination
of P. pseudofuligineum and Muntingia was apparently
more attractive to bats than P. amalago alone. We
postulate that Glossophaga soricina is the bat primar-
ily responsible for removing fruits from the poles since
it is a major dispersal agent of these species and also
consumes fruits of Piper (Table 4).
Chlorophora tinctoria.-For unknown reasons, the
control (= fruits under or in a vertical transect in a
fruiting tree) did not work in this species' experiments.
A significantly higher (P < .05) percentage of fruits
placed in nonresource areas was taken than the control
fruits (Table 6). We cannot explain these results. In the
presence of Piper pseudofuligineum (and also Muntin-
gia calabura) in nonresource areas, a much higher
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Ecology, Vol. 58, No. 3
percentage of C. tinctoria fruits was taken. The bat
most likely to produce this result is Carollia perspicil-
lata (Table 4). We do not know why this species and
Artibeus jamaicensis, the two major bat dispersers of
this fruit, did not remove the control fruits.
Muntingia calabura.-Results of the relocation ex-
periments were similar to those of Ficus: a signifi-
cantly higher percentage of the "resource area" fruits
was taken than the "nonresource area" fruits
(.025 > P > .01). Away from Muntingia trees in the
presence of Piper pseudofuligineum (and Chlorophora
tinctoria), the removal percentage also increased mark-
edly (Table 6). Since it consumes fruits of all three
species, Carollia perspicillata is the most likely re-
moval agent in these experiments.
DISCUSSION
Results of these experiments indicate that bats differ
in their sensitivity to fruits that have been moved away
from nonspecific plants. Bats found relocated fruits of
two Piper species much more readily than they did
relocated fruits of two species of Ficus and Muntingia
calabura. The probability that fruits of Ficus ovalis,
Chlorophora tinctoria, and M. calabura would be lo-
cated by bats was significantly increased by being in
the presence of Piper pseudofuligineum fruit. These
findings are consistent with the hypothesis that certain
bats (especially Carollia perspicillata and Glos-
sophaga soricina) are constantly "on the alert" for
ripe Piper fruits whereas bats that eat Ficus fruits
(e.g., Glossophaga soricina andArtibeusjamaicensis)
are not constantly "on the alert" for these fruits. Bats
that eat Piper fruits must occasionally search for these
fruits while commuting whereas those feeding on
Ficus or Muntingia apparently do not search for these
fruits while commuting.
These results appear to correlate with the density
and dispersion patterns and phenology of the various
species of Piper and Ficus and Muntingia calabura at
Santa Rosa. Ripe Piper fruits occur at low nightly den-
sities on scattered individuals or in patches containing
a few to many individuals located in a variety of
edaphic and successional areas. Owing to the cyclical
pattern of fruit production within Piper species and
displaced fruiting cycles between species, these fruits,
which appear to be highly preferred by Carollia
perspicillata, are available throughout the wet season
and, judging from our observations at La Pacifica
(Heithaus et al. 1975), during parts of the dry season.
To maximize its searching efficiency for these fruits,
which are clearly a limited resource because bats re-
move nearly all ripe fruits the first night they are avail-
able, C. perspicillata, as well as Glossophaga soricina
and perhaps other species, has apparently developed
sensitive olfactory/visual search images for Piper
fruits. In addition to being of obvious selective advan-
tage to the bats, this sensitivity is advantageous to
species of Piper because it means that the fruits of
Late Spring 1977 FOOD LOCATION BEHAVIOR IN FRUGIVOROUS BATS
most plants, whether they occur as members of large
patches or as scattered individuals, will be found and
their seeds dispersed by bats.
The density, dispersion, and phenology of species of
Ficus differ markedly from that of Piper in that large
numbers of fruits are produced asynchronously by
widely-scattered individuals over relatively short
periods of time. Ficus fruits are thus much more patch-
ily distributed in space and time than Piper fruits,
which is why we initially predicted that bats would
commute directly to areas containing these fruits. This
prediction was upheld by the results of our experi-
ments, which implies that as bats such as Glossophaga
soricina, Artibeus jamaicensis, and perhaps others fly
through a habitat they are not constantly sensitive to
Ficus fruits. Instead, they first fly to known trees be-
fore searching for ripe fruits. Since individuals of both
species of Ficus fruit asynchronously, it is likely that
bats feeding on these species must spend considerable
time and energy scouting out the locations of ripening
fruit crops. Morrison's (1975) observations of the
foraging behavior of Artibeus jamaicensis on Barro
Colorado Island, Panama Canal Zone, where most of
its diet is based on fruits of several species of Ficus,
indicate that scouting behavior is indeed an important
component of its foraging strategy.
Although it fruits year-round, Muntingia calabura is
very patchily distributed in space. As in the case of
Ficus, bats should be expected to search for ripe Mun-
tingia fruits only after they have arrived at a clump of
trees. Results of the relocation experiments indicate
that this is the case and suggest that bats feeding on
Muntingia are not sensitive to ripe fruits until they
have first located a fruiting tree.
Two main conclusions arise from this study. First,
depending on the spatial distribution of their food,
some species of bats may commute directly to a feed-
ing area before beginning to search for food (a "sepa-
rate" strategy) while other species search and commute
simultaneously (a "mixed" strategy). The strategy
used is consistent with optimizing energetic (or time)
return for unit of effort expended. Species with
relatively broad diets (e.g., Carollia perspicillata and
Glossophaga soricina) probably use a "mixed" strat-
egy when their preferred food is moderately patchy, as
is Piper. In contrast, Artibeus jamaicensis, a bat with a
more restricted diet at Santa Rosa, specializes on food
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627
that is restricted to productive but ephemeral patches
and consequently does not search and commute simul-
taneously. Secondly, the strategy used depends more
on the food used at a particular time then on the bat
species in question. Bats may "switch" from simul-
taneous commuting and searching to temporally
separating these behaviors when different resources
are being eaten. For example, Glossophaga soricina
appears to use a "mixed" strategy when feeding on
Piper, but a "separate" strategy when feeding on
Ficus ovalis. Our overall conclusion is that the food
location behavior of frugivorous bats appears to be
highly responsive to differences in the spatiotemporal
distribution patterns of their food resources.
ACKNOWLEDGMENTS
We thank the directorsof the Costa Rican National Park
Service (Ings. MarioBoza and AlvaroUgalde)for permission
to conduct our research at Santa Rosa. Sr. Guillermo
Canessa,biologicaldirectorat the park,extendedmanycour-
tesies and muchhospitalityduringour work there. We thank
Bob Rauscherand Ed Stashkofor theirassistancein the field.
We also thankAl Covich, Brock Fenton, Bob Jamieson,and
Bob Sussmanfor discussion and commentson draftsof this
paper. The research was supported by summer research
grantsfrom the University of Missouri-St.Louis and North-
western University and by NSF grantDEB 75-23450.
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