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of the
FLORIDA STATE MUSEUM
Biological Sciences
Volume 24 1979 Number 4
FORAGING AND REPRODUCTIVE ECOLOGY IN A
PANAMANIAN BAT COMMUNITY
FRANK J. BONACCORSO
UNIVERSITY OF FLORIDA
GAINESVILLE
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Publication date: December 20, 1979
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FORAGING AND REPRODUCTIVE ECOLOGY IN A
PANAMANIAN BAT COMMUNITY
FRANK J. BONACCORSO'
SYNOPSIS: Resource partitioning, reproduction, and community structure in a tropical
moist forest community of 35 bat species were studied on Barro Colorado Island,
Panama Canal Zone. Over a three-year span 2884 bats were captured, banded, and
released; data were collected on food habits, activity cycles, habitat selection, and
reproductive timing. Information on seasonality and abundance of fruit, flower, and in-
sect resources used by bats also was collected.
Fluctuating levels of food resources require that many bat species utilize different
habitats and foraging strategies through a year. Competitive interactions, predator
avoidance, and climatic fluctuations further influence foraging strategies. The bat com-
munity is divided into nine feeding guilds on the basis of diet and method of food pro-
curement. Within the most complex guilds food resources are partitioned temporarily,
specially, and by size and quality. Within the simplest guilds food resources are parti-
tioned primarily by particle size.
Reproduction coincides with high levels of food availability. Species utilizing food
sources abundant over most of the year have two litters per year.
TABLE OF CONTENTS
INTRODUCTION .................................... .................. 360
ACKNOWLEDGEMENTS .. .... ..................................... 361
STUDY AREA .... ............. .............................. ....... 361
M ATERIALS AND M ETHODS ............................................... 361
PHENOLOGY OF FOOD RESOURCES ......... ...................... .......... 363
RESOURCE PARTITIONING ... ....... ........... . .. ................... 365
CANOPY FRUGIVORE GUILD ............. ......... .................. 368
GROUNDSTORY FRUGIVORE GUILD .......... .......................... 377
SCAVENGING (OR JUICER) FRUGIVORE GUILD ............... ............ 380
NECTAR-POLLEN-FRUIT-INSECT OMNIVORE GUILD ........................ 381
SANGUIVORE GUILD ............. ....................... ......... 383
GLEANING CARNIVORE GUILD ....................................... 385
SLOW-FLYING HAWKING INSECTIVORE GUILD ............... ........... 388
REPRODUCTION ........... .... .. ........... .............. .......... 390
CANOPY FRUGIVORE GUILD ........... ............................... 391
GROUNDSTORY FRUGIVORE GUILD .......... ....... ................... 393
SCAVENGING FRUGIVORE GUILD ................... ................ 394
NECTAR-POLLEN-FRUIT-INSECT OMNIVORE GUILD ....................... 394
SANGUIVORE GUILD ...................................... ......... 394
GLEANING CARNIVORE GUILD ................. ................... 395
SLOW-FLYING HAWKING INSECTIVORE GUILD ............... ........... 396
DISCUSSION............. ............ .................................. 397
DIVERSITY AND PHENOLOGY ................... .................. 397
FORAGING AND REPRODUCTIVE STRATEGIES ............... ............ 399
LITERATURE CITED ................... .......... .................... .. 406
'The author is Adjunct Assistant Professor, Biology Department, University of Wisconsin-Eau Claire, Eau Claire,
Winconsin 54701. This study was submitted as partial fulfillment of the Ph.D. degree in the Department of Zoology,
University of Florida, Gainesville, 32611.
BONACCORSO, FRANK J. 1978. Foraging and Reproductive Ecology in a
Panamanian Bat Community. Bull. Florida State Mus., Biol. Sci. Vol. 24(4):359-408.
BULLETIN FLORIDA STATE MUSEUM
INTRODUCTION
The words "tropical forest" typically engender visions of species-
rich communities, complex competitive interactions, and relatively
stable environments. Indeed, faunal lists in the tropics are large, and
food webs are intricately complex. It is also true that organisms in-
habiting tropical lowlands usually are subjected to less extreme en-
vironmental fluctuations than are their counterparts in temperate or
polar regions. However, it is too infrequently emphasized that even
species in tropical forests must possess behavioral flexibility to
counter and survive climatic and biotic environmental change. There
are two major reasons for this oversight. First, few detailed studies of
tropical organisms have spanned periods of several years or even
seasons, and second, behavioral responses of tropical species to en-
vironmental fluctuations are often quite subtle. Whereas temperate
animals commonly exhibit obvious and dramatic responses to seasonal
change such as hibernation or long distance migration, tropical species
may need only to switch food types or microhabitats, or briefly halt
reproduction (Kaufmann 1962, Wolf 1970, Mares and Wilson 1971a,
Snow and Snow 1972, Orians 1973, Montgomery and Sunquist 1973).
Nevertheless, genetic and behavioral flexibility are requisites of sur-
vival for most tropical as well as temperate species.
Tropical bats are particularly good subjects for studies of diversi-
ty, competitive interaction, and response to environmental fluctuation
because of their individual abundance and the complex taxonomic and
ecological communities they form. About 100 species of bats occur in
each of the small countries of Central America (Hall and Kelson 1959).
It is common to find 30 to 50 species in one macrohabitat measuring a
few square kilometers in area.
Among tropical bat species, few are known or suspected to
reproduce year round or to specialize on constantly abundant food
resources; the common vampire bat, Desmodus rotundus, being a
notable exception on both counts (Wimsatt and Trapido 1952, Turner
1975). Most bats in equatorial regions are seasonally polyestrous or
monestrous in reproduction (Baker and Baker 1936, Mutere 1970,
Fleming 1973) and make seasonal shifts in diet (Wilson 1971b, Flem-
ing et al. 1972, Heithaus et al. 1974).
The objective of this paper is to delineate adaptive strategies used
by tropical bats that enable them to survive and reproduce under fluc-
tuating environmental conditions and coexist with numerous similar
species in complex communities. The field work represented herein
documents seasonal changes in food resources, mechanisms of
resource partitioning, and reproductive timing through one complete
year and portions of two other years.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
ACKNOWLEDGEMENTS
This study was funded by NSF Grant GB-36068 to J. H. Kaufman, NIH Biomedical
Sciences Grant No. RR7021-07 from the Division of Sponsored Research, University of
Florida, to S. R. Humphrey, and the Environmental Sciences Program, Smithsonian
Tropical Research Institute. The Florida State Museum and Smithsonian Tropical
Research Institute provided logistical support.
B. K. McNab, both in his writings and classroom d' 2cussions, induced and encour-
aged the germ plasm of interest that launched me into the study of the ecology of
tropical bat communities. S. R. Humphrey provided help and encouragement through
all phases of the study, including assistance with field work in January 1973. J. H.
Kaufmann, E. Leigh, A. S. Rand, N. Smythe, A. F. Carr, D. H. Hirth, and T. C. Emmel
took time to provide constructive guidance. Robin Foster verified my seed identifica-
tions and cultured in me a deep appreciation for tropical plant ecology. Clark Sandford,
Julie Wiatt, Bill Biven, and Janet Hall faithfully assisted with fieldwork and laboratory
preparations under trying conditions. Nancy Halliday and Sylvia Scudder used their
creative talents to render the illustrations. Insects eaten by bats were identified by
Terry Zinn. Finally, I wish to thank the scientists, students, and visitors coinciding
with my residence on BCI, as well as the Smithsonian staff, for providing encourage-
ment, friendship, intellectual atmosphere, and volleyball at an isolated field station.
STUDY AREA
The primary research site was Barro Colorado Island (BCI), which lies within
freshwater Lake Gatun, Panama Canal Zone, at 90 10' N Lat, 790 51' W Long. This site
was selected because it has a rich bat fauna, relatively undisturbed mature moist
forest, modern living and laboratory facilities, and reference collections of animals and
plants. A second site was located on the mainland opposite BCI at the base of Buena
Vista Peninsula (Fig. 1).
The climate of this lowland area of Panama is warm and humid, with a 7-month (May
through November) wet season and a 3-month (January through March) dry season.
Dry season months each receive less than 60 mm of rain, whereas wet season months
typically receive in excess of 250 mm of rain. April and December are transition months
between the dry and wet seasons and receive amounts of rain that vary considerably
from year to year. Thus in years when April and December are very dry, the dry season
may last for five months. Average annual rainfall since 1926 has been 2820 mm
(Smythe 1974). Monthly sums of rainfall for 1973 are shown in Figure 3.
During night-time sampling of bats, relative humidity under the forest canopy never
fell below 80 percent. Measurements were made at 2 m above ground with sling
pyschrometer. Daily temperatures on the forest floor fluctate from a mean minimum of
22.1C to a mean maximum of 28.0"C, with no significant seasonal variation (Smythe
1974).
Barro Colorado is in the Tropical Moist Forest life zone (Holdridge 1967). This 15
km2 island is covered with forest that is over 60 years in age. The only physical disturb-
ance results from recutting forest trails, maintaining a small laboratory clearing, and
an undetermined amount of poaching. Further details on the geology, climate, biology,
and history of the island are given by Kaufmann (1962) and Foster (1973).
MATERIALS AND METHODS
There were 17 sampling stations in an approximately 2 km2 central strip of BCI and
one station on Buena Vista Peninsula (Fig. 1). Habitats sampled during the study were
classified as mature forest (14 stations on BCI), creeks (3 stations on BCI), and second
BULLETIN FLORIDA STATE MUSEUM
growth (1 station on Buena Vista). The mature forest, a minimum of 60 years old in all
places, had a completely closed canopy. Creeks were lined with rich shrub growth and
the creek beds received direct sunlight. Second-growth habitat at Buena Vista was ap-
proximately 20 years old and consisted of thick shrub growth and scattered small trees
that formed a discontinuous canopy.
Each sampling station consisted of four or six 6 x 2 m mist nets and one or two
Tuttle harp traps (Tuttle 1974) set across permanent trails. Nets were set in pairs at
100 m intervals, with one of each pair at ground level (0-3 m) and the other at subcanopy
and lower canopy level (3-12 m). Early in the study nets were rigged in the canopy as
high as 25 m above ground, but use of these nets was soon discontinued because few
bats were captured in them, which seemed to reflect little flight activity in the canopy.
Harp traps were usually set at ground level in low, narrow tunnel-like passages created
by vegetation and trails. At a few stations where the vegetation permitted, harp traps
were rigged in subcanopy level "tunnels."
Nets and traps were open from sunset to sunrise 67 times between 11 January and
31 December 1973. On 28 other nights during that period, sampling was conducted for
less than a full night. Total sampling during 1973 involved 4376 net-hours, 1213 trap-
hours, and 2324 captured bats.
In 1971, a pilot study of 347 net-hours yielded 282 bats between 20 June and 18
August. In 1974 between 10 June and 17 July, 454 net-hours of additional sampling
yielded 278 bats. No harp traps were available during these times.
FIGURE 1.-Barro Colorado Island study area showing the 17 sampling stations.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
Crespo et aL (1972) and Morrison (in press) have demonstrated that vampires and
fruit bats avoid flying during intense moonlight. Whole-night samples were taken only
between the last and first quarter of the moon. Thus activity cycles were measured dur-
ing phases of the lunar cycle that did not produce enough light to influence bat flight
activity.
Nets and traps were checked at least twice every hour. When possible net checks
were made more frequently to prevent bats from chewing out of nets. Upon removal
from a net or trap each bat was placed in an individual cloth bag. Usually within an
hour after capture the bats were banded, as described in Bonaccorso et al. (1976), and
released at the sampling station. The following data were recorded for each individual:
species, hour and location of capture, sex, age class, reproductive condition of females,
food in feces or mouth, weight, and forearm length.
Age classes were distinguished as follows: infants were unable to fly and were en-
countered only when carried by the mother; juveniles were able to fly but still had the
infant pelage; subadults had the adult pelage but were smaller in weight than adults
and were reproductively immature; adults possessed both adult pelage and weight.
Pregnancy, lactation, and reproductive inactivity of adult females were determined
by palpation. Additionally, females could be distinguished as nulliparous or post-
lactating by examining the condition of the teats.
Fecal pellets obtained from individual animals were placed in separate glassine
envelopes for laboratory identification of food species. Fruits and pollens in fecal pellets
were identified to species by comparing unknowns with seeds, pulp fibers, and pollen
grains in a reference collection I assembled. Pellets collected from insectivorous bats
are in the process of analysis, and this information will be published elsewhere. Pollen
on the fur was collected by swabbing with a gelatin as described by Beattie (1971). The
pollen-containing gelatin was then melted on slides for microscopic identification. In
calculating feeding niche breadths and overlaps the fecal pellets in a single glassine
envelope were scored as a sample of one for the given food species it contained (pollen or
fruit). For the stenodermine fruit bats the fecal pellets from a single defecation seemed
to represent part of a single fruit that was eaten. Food passage along the digestive tract
is very rapid (Klite 1965), and a given defecation probably represents the last fruit
eaten by the bat. For carolline bats a single fecal pellet sometimes contained two types
of seeds. This probably resulted from eating very small fruits and switching food
species within very short intervals.
Occasionally animals were captured with whole fruits held in the mouth. Additional
information on food habits was gathered by placing plastic sheets under two roost trees
of Carollia perspicillata to gather discarded fruits and fecal matter.
Niche breadth is calculated as log, B = Ep, log, p,, where p, is the number of the i'
food species divided by sample size (Levins 1968). Values approaching zero indicate nar-
row niche breadths and specialists. Values approaching one indicate niche breadths of
generalists. Niche overlap is calculated as CX = 2EX,/EX, + Y,, where X, is the propor-
tion of the i'" food species in the diet of bat species X, and Y, is the proportion of the i'
food species in the diet of bat species Y (Morista 1959). I follow Zaret and Rand (1971) in
considering species with overlap values greater than 0.6 to be critically similar in terms
of food overlap.
PHENOLOGY OF FOOD RESOURCES
Most of the bat species on BCI depend largely on fruit, flowers, or
insects as food resources. Only a few species eat flesh or blood of
vertebrates or non-insect invertebrates. The abundance and diversity
1979
BULLETIN FLORIDA STATE MUSEUM
of fruits, flowers, and insects in Central America, even in Moist and
Wet Forests, show marked seasonal fluctuations (Foster 1973, Smythe
1974, Frankie et al. 1974, Morrison 1978).
Pollen and nectar on BCI are available to bats as reliable food
sources only in the dry season, and only four species of flowering
plants are known to be used by bats (Fig. 2). Two common species,
Ochroma lagopus and Pseudobombax septenatum, flower from mid-
December to mid-March. While these two species are in bloom, nectar
and pollen are very abundant. The other two pollen types used by bats
remain unidentified. One of these is known only from February to
March and the other from August to September.
Fruits from 45 plant species were eaten by bats on BCI (Fig. 2).
These included 19 trees, 11 shrubs, 4 vines, 4 epiphytes, and 7 undeter-
mined. Mature fruits were available to bats all year, but most species
bearing fruits eaten by bats produced ripe fruits for periods of only one
to four months. Only Ficus insipida, F. obtusifolia, and F. yoponensis,
have ripe fruits available nine or more months per year. Individuals in
the populations of these fig species fruit asynchronously one to four
times per year. F. insipida and F. yoponensis populations show two
major fruiting peaks and troughs each year (Morrison 1978). Ripe figs
are scarce in March and again from late August until late November.
The plant genera Cecropia, Spondias, Vismia, and Piper have two
or more bat-dispersed species that set fruit in sequential time periods
(Fig. 2). Ten species of pipers are eaten by bats on BCI. Though none of
these species is available for more than a few months, two or more
species have ripe fruit at any one time through the year. Pipers also are
important bat fruits in Costa Rica where several species fruit in se-
quential series (Heithaus et al. 1974).
During 1973 a maximum of 19 fruiting species was available from
mid-March to mid-April, and a minimum of 6 species was available in
November-December (Fig. 2). Two of the fruits available in November-
December, Ficus insipida and F. yoponensis, were relatively scarce,
but Spondias radlkoferi and S. mombin were very abundant.
Biomass and numbers of nocturnal insects caught in light traps in
Barro Colorado forest over a 3-year period were reported by Smythe
(1974). Though these samples represent all nocturnal flying insects,
they provide a useful index of abundance and fluctuations of the poten-
tial food resources for insectivorous bats. Smythe's light trap collec-
tions showed that nocturnal insect biomass in the early wet season is
as much as eight times that at the end of the wet season and during the
dry season (Fig. 3). Large insects (> 5 mm length) were responsible for
this seasonal change in biomass, with Isoptera, Diptera, and
Lepidoptera among the orders eaten by bats that have particularly
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
dramatic population increases in the wet season. By contrast, small in-
sects (< 5 mm length) were abundant throughout the year.
RESOURCE PARTITIONING
Of 35 species of bats captured or sighted on BCI in 1973, 31 species
were captured in nets or traps and 4 other species were seen in flight or
at roosts. Noctilio leporinus, N. labialis, and Molossus molossus ap-
peared to be abundant but restricted their flight activities to habitats
not sampled-the shallow inlets of the lake (Noctilio) and above the
forest canopy (Molossus). The fourth species not captured, Vampyrum
spectrum, is a top carnivore and may be represented by very few in-
dividuals on the island. A pair of V. spectrum was netted by A. L.
Gardner and D. E. Wilson on 5 January 1973. In June 1973 I saw a
single animal flying at dawn.
A first step at understanding how 35 species of bats partition food
resources on this small island can be made by dividing the fauna into
feeding guilds distinguished on the basis of two parameters-diet and
method or place of food procurement. This permits examination of
small complexes of species with similar foraging behaviors and diets. I
have divided the bats on BCI into nine feeding guilds with one to nine
species per guild. Justification for the placement of species into
specific feeding guilds will be provided in succeeding sections. For the
moment, the guilds are defined as follows:
(1) "Canopy frugivores"-forage mostly on fruits that grow in the
trees of the canopy and subcanopy level of the forest, above 3
m from the ground.
(2) "Groundstory frugivores"-forage mostly on fruits of
shrubby groundstory plants, 0 to 3 m above ground level.
(3) "Scavenging frugivores (or juicers)"-feed mostly on very soft
ripe fruit, and/or over-ripe fruit.
(4) "Nectar-pollen-fruit-insect omnivores"--forage for pollen and
nectar when available during the dry season and for fruits and
insects at other times.
(5) "Sanguivores"-feed only on the blood of mammals and birds.
(6) "Gleaning carnivores"-forage for small animals (arthropods
or vertebrates) that are perching or moving on vegetation or on
the ground.
(7) "Slow-flying hawking insectivores"-forage for flying insects
in small openings beneath or in the forest canopy or over
streams.
(8) "Fast-flying hawking insectivores"-forage for flying insects
above the forest canopy or in very large open spaces (e.g.
pastures).
1979
PLANT SPECIES
PLANT
TYPE JAN FEB MAR APR MAY JUNE JULY AUG SEPT OCT NOV DEC
FLOWERS
Ochroma lagopus
Pseudobombax septenatum
Unknown 201
Unknown 202
FRUITS
Ficus insipida
F obtusifolia
E popenoaei
F yoponensis
F 102
Spondias mombin
S. radlkoferi
Dipteryx panamensis
Calophyllum longifolia
Quararibea asterolepsis
Cecropia eximia
C. obtusifolia
Anacardium excelsum
Solanum hayesii
Vismia species 1
Vismia species 2
Astrocaryum standleyanum
Tetrathylacium johanseni
Poulsenia armata
Cassia undulatum
Market panamensis
Clusia odorata
Unknown 126 (Passifloraceae)
Unknown 101 (Araceae)
Unknown 103 (Araceae)
Aechmea tillandsiodes
Im
am E
M M 2E H MHimmmmm HM ll
f'-- -/
m m i I H M
~gg-g-
----- - - -Eg -
- -
-m- -
1-7 -
m-- m
mnm
mmERmngmm
a m ggggm m mgg
-m
mI
Fggg a
-m ----
mnmg
- m mm-m
--m
Carludovicia palmata
Havetiopsis 125
Piper aequale
P. carriloanum
P cordulatum
P marginatum
R reticulatum
Piper 109
Piper 114
Piper 116
Piper 120
Piper 122
Unknown 104
Unknown 110 (Cucurbitaceae)
Unknown 127
Unknown 131
Unknown 117
Unknown 124
Unknown 130
TOTAL NUMBER OF FOOD
PLANT SPECIES AVAILABLE
m -m
m
m m m ngg
m m-
-m
m m-
U
9 15 17 19
- -
- 0
- 8
>
I >
z
z
17 12 15 10 11 7 8 6 12 -
FIGURE 2.-Monthly availability of fruits and flowers used by bats on Barro Colorado Island. Solid bars indicate food present in fecal
samples. Striped bars indicate food known to be available, but not present in fecal samples. Empty bars indicate probable availability of
food. Lunar months begin about the 12th day of each calendar month. Plant types: T = tree, S = shrub, V = vine, E = epiphyte, U =
unknown.
BULLETIN FLORIDA STATE MUSEUM
DRY SEASON WET SEASON
J F M A M A S O N D
MONTH
FIGURE 3.-Schematic representation of fluctuation in biomass of nocturnal flying in-
sects through the year (Based on samples from three years, after Smythe 1974). Bars
represent rainfall in millimeters.
(9) "Piscivores"-forage for fish or aquatic invertebrates at or
just above the surface of lakes and large streams.
CANOPY FRUGIVORE GUILD
BODY SIZE.-Eight species, all in the subfamily Stenoderminae of
the family Phyllostomatidae, constitute the canopy frugivore guild on
BCI. These eight species range from 8.1 to 69.3 g in mean body weight
(Table 1.). There is a mean increment of 1.44 between the body weights
of adjacently sized animals designated as fig specialists. Artibeus
TABLE 1.-WEIGHTS OF CANOPY FRUGIVORE BATS ON BCI.*
Species X S.D. n Wgt/wgt,, Remarks
V. pusilla 8.1 0.6 22 common, fig specialist
C trinitatum 12.3 1.2 7 1.53 very rare, fig specialist
A. phaeotis 13.0 1.2 30 common, fruit generalist
V. helleri 16.2 2.2 8 1.31 very rare, fig specialist
C. villosum 22.4 2.1 13 1.38 rare, fig specialist
V. caraccioloi 36.0 2.3 27 1.61 common, fig specialist
A. jamaicensis 47.2 3.4 30 1.31 superabundant, fig specialist
A. lituratus 69.3 5.6 30 1.47 common, fig specialist
mean ratio of weight increment = 1.44
*X = mean weight in grams; S.D. = standard deviation; n = sample size; Wgt/Wgt,. = weight of species divided by
weight of next smallest species.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
phaeotis, a feeding generalist, and Chiroderma trinitatum are nearly
equal in size.
FOOD SELECTION.-All eight canopy frugivore species feed pri-
marily on fruits of large canopy and subcanopy trees, in particular figs
of the genus Ficus. Over 60 percent of the annual diet (by frequency of
occurrence of fecal pellets containing a given species of plant seeds) of
the seven fig specialists consists of fig fruits (Table 2). A. phaeotis
depends on figs for only 30 percent of its diet. Five species of Ficus, all
of which are green-colored at maturity, are eaten and dispersed by
these stenodermines on BCI. Fig trees that produce small fruits like F.
yoponensis and F. popenoaei are preferred by small bat species, and
trees that produce larger fruits like F. insipida and F. obtusifolia are
preferred by the larger bats.
Figs form the bulk of the diet of Artibeus jamaicensis throughout
most of the year. However, during the latter part of the wet season and
the beginning of the dry season mature fig fruits are very scarce (Mor-
rison 1978). At this time A. jamaicensis turns more heavily to other
fruits and pollen (Table 3). The relative importance of pollen in the diet
of A. jamaicensis may be underestimated in Table 3, because my
sampling schedule did not coincide precisely with the period in late
December and early January when figs were very scarce and flowers
were very abundant. Similar seasonal switches in diet also probably
occur for A. lituratus and V. caraccioloi, but the data are weak. No con-
clusions are made from the scant data on the smaller canopy
frugivores about seasonal changes in diet.
Unlike fig specialists, A. phaeotis eats a more even distribution of
many types of fruits (Table 2 and 3) with no one species dominating
the diet. Throughout the year figs are a minor component of the diet,
while other fruits are very important in certain months. Cecropia
eximia is an important food item from July to September, as is Spon-
dias radlkoferi in November to January.
TABLE 2.-PERCENT OF DIET FROM MOST IMPORTANT FOOD PLANT GENERAL AND SPECIES
TAKEN FROM FECAL SAMPLES OF BATS IN THE CANOPY FRUGIVORE GUILD.
Percent most Most Important Number of fecal
Bat species important genera* species samples
V. pusilla 92 Ficus F. yoponensis 13
C. trinitatum 60 Ficus F. popenoaei 5
A. phaeotis 30 Ficus Spondais radlkoferi 33
V. helleri 67 Ficus F. insipida 6
C. villosum 100 Ficus F. popenoaei 6
V. caraccioloi 76 Ficus F. insipida 17
A. jamaicensis 78 Ficus F. insipida 185
A. lituratus 65 Ficus F. insipida 20
*By frequency of occurrence as explained in Materials And Methods.
BULLETIN FLORIDA STATE MUSEUM
TABLE 3.-BIMONTHLY SAMPLES OF IMPORTANT FOOD GENERA IN DIETS OFArtibeus AND
Vampyrodes. NUMBERS INDICATE FECAL SAMPLES WITH A GIVEN FOOD
PRESENT. SAMPLING PERIODS BEGIN AT MID-MONTH.
Food species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan
Artibeus jamaicensis
Ficus spp. 18 25 25 35 21 17
Cecropia spp. 3 3
Spondias spp. 1 8 6
Quararibea 9
Pollen 1
Total fecal samples* 20 30 32 39 35 37
Artibeus lituratus
Ficus spp. 2 4 2 1 4
Spondias spp. 1 1 1
Pollen 1
Total fecal samples* 3 4 5 2 7
Artibeus phaeotis
Ficus spp. 2 1 2 1 3
Cecropia spp. 1 5
Spondias spp. 8
Total fecal samples* 5 6 9 1 11
Vampyrodes caraccioloi
Ficus spp. 1 2 4 3 1
Pollen 2
Total fecal samples* 3 3 4 3 2
*Includes genera of lesser importance not shown here.
Feeding niche breadths based on frequency of occurrence of food
species in the diet are presented in Table 4. Large niche breadth values
represent food generalists and small values food specialists. A.
phaeotis stands alone at the generalist extreme of this index. Among
the other species, A. jamaicensis has an intermediate position;
TABLE 4.-FEEDING NICHE BREADTHS OF CANOPY FRUGIVORES. SAMPLE SIZES FOR
CALCULATING NICHE BREADTHS ARE FROM TABLE 2.
Genera of known Species of known Niche breadth
Bat species food plants food plants (log. B)
V. pusilla 2 4 0.94
C. trinitatum 3 4 1.33
A. phaeotis 10 12 2.10
V. helleri 2 3 1.01
C. villosum 1 3 1.01
V. caraccioloi 4 5 1.04
A. jamaicensis 9 16 1.61
A. lituratus 5 7 1.33
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
however, the very narrow niche breadths of the other specialists seem
to be the result of small samples in calculating niche breadths. There is
a significant positive correlation between sample size and the number
of plant species in Table 4 (r = 0.865).
Niche overlap in food species is compared in Table 5. The highest
values of overlap occur between species most similar in size. A.
phaeotis overlaps little with all the fig specialists, except for V. helleri,
which is similar in size to A. phaeotis. The high values of overlap be-
tween many of the fig specialist species indicate that some mechanism
other than selection of food species must reduce behavioral in-
terference and/or interspecific competition for food in this guild if food
is a limiting factor.
Several types of evidence suggest that, at least during some parts
of the year, food is a limiting factor for fruit bats on BCI. The biomass
of fruit and the number of species of fruiting trees fluctuate quite
drastically on a seasonal basis (see Phenology section). During the late
wet season fruit availability is low, and an increased proportion of cap-
tured fruit bats have empty stomachs (83% in Oct-Nov) as compared
to times of fruit abundance (71% in Mar-Apr). Also in the late wet
season various other frugivorous mammals come to the laboratory
clearing with increased frequency to seek food (Foster 1973). By the
late wet season several species of fruit bats have temporarily moved
out of the study area in response to low food levels (Bonaccorso and
Humphrey, in prep.). Even when fruit is very abundant in terms of
total biomass, many types are concentrated in a limited amount of
space, the few trees fruiting at any moment, and may still be a limiting
factor for population size.
VERTICAL STRATIFICATION..-Handley (1967) and Harrison (1962)
TABLE 5.-FEEDING NICHE OVERLAPS (C) AMONG SPECIES OF CANOPY FRUGIVORES.
LOWER DIAGONAL INDICATES OVERLAP BETWEEN FIG SPECIALISTS MOST
SIMILAR IN SIZE.
0 5
A. phaeotis .215 .345 .615 .241 .465 .485 .518
V. pusilla .968 .452 .796 .679 .272 .152
C trinitatum .893 .743 .644 .209 .412
V. helleri .798 .886 .852 .452
C. villosum .727 .200 .310
V. caraccioloi .994 .962
A. jamaicensis .983
1979
BULLETIN FLORIDA STATE MUSEUM
demonstrated a vertical stratification of flight activity in tropical bat
species, with most canopy frugivores preferring upper levels of the
forest. On BCI V. pusilla, A. phaeotis, C. villosum, V. caraccioloi, and
A. lituratus were captured with significantly greater frequency in the
nets and traps set above 3 m (Table 6). V. helleri and C. trinitatum also
were captured most frequently in subcanopy and canopy levels, but
samples sizes for these species are small, and frequency differences are
not statistically significant. A. jamaicensis is the only species of the
guild to show a significant preference for activity at the groundstory
level, yet 42 percent of the captures of this species too were in the
upper levels of the forest. Though most of its food items grow in the
upper levels of the forest, A. jamaicensis may fly close to the ground to
avoid predators, or because it is more efficient for a large bat to fly
along cleared trails than to echolocate and avoid the dense vegetation
above. At any rate this behavior seems an artifact of human manage-
ment of the forest.
HABITAT SELECTION.-Comparison of netting samples from the
young open forest of Buena Vista and the mature closed canopy forest
and creek habitats is presented in Fig. 4. As a group fig specialists are
much more common in closed forest and creeks lined by closed forest
than in shrubby open forest where few mature trees of their preferred
food species are found. A. phaeotis and A. jamaicensis are common to
very abundant in all three habitats, as would be expected from their
generalized food requirements. Except for A. jamaicensis, none of the
fig specialists are common on Buena Vista Peninsula.
FEEDING BEHAVIOR.-Canopy frugivores usually carry fruits by
mouth from fruiting trees to night roosts (Goodwin and Greenhall
1961, Morrison 1978). On BCI Morrison found that the night roosts of
TABLE 6.-VERTICAL STRATIFICATION OF CANOPY FRUGIVORES. STATISTICAL
SIGNIFICANCE INDICATES PREFERENCE FOR ONE OF THE Two VERTICAL
STRATA. YATES CORRECTION FOR CONTINUITY Is USED FOR ALL TESTS OF
SAMPLES WITH N < 200 (Sokal and Rohlf 1969).
No. of bats captured at No. of bats captured at
Bat species ground level, 0 to 3 m subcanopy levels, 3 to 12 m
V. pusilla 5 25**
C. trinitatum 2 4
A. phaeotis 36 56*
V. helleri 3 6
C. villosum 4 24**
V. caraccioloi 4 30**
A. jamaicensis 467** 326
A. lituratus 23 66**
*Significant by Chi Square Test (P < .05)
**Highly significant by Chi Square Test (P < .01)
372
Vol. 24, No. 4
-Itm2Tm
SECOND GROWTH
5 I 2 15 139 32118132 12 6102236
~1 32 12 651
CREEKS
MATURE FOREST
I II l i I l I II I ! I l I I
9 '32' 2 '10'5 '13' 8' 7'17' 1 3 '19'21'26'29'16'20' 6'18'4 '22'30'23'28'15'12'11'14'
FIGURE 4.-Relative abundance of bat species in three habitats. Numbers along horizontal axes refer to species as assigned in Fig. 16.
o I I I
BULLETIN FLORIDA STATE MUSEUM
A. jamaicensis are frequently several hundred meters from the trees
where fruits are picked. Only when feeding on fruits of Dipteryx
panamensis did A. jamaicensis feed in fruiting trees, apparently
because Dipteryx fruits are too large for this species to carry effi-
ciently (pers. obs.). Vampyrodes caraccioloi, A. jamaicensis, A.
lituratus, and A. phaeotis were observed carrying whole or partially
eaten fruits in flight. These animals were transporting food items to a
night roost for consumption. It was not determined whether the less
common guild members use night roosts as eating sites.
Fruits carried in flight by fruit bats vary in weight from less than 1
g to about 20 g. Most bats carry fruits that weigh 20 to 40 percent of
their own body weight. Table 7 lists the range in weight of some fruits
eaten by stenodermine bats. There is considerable variation in the
weights among and within species for these fruits (even in fruits from
an individual tree).
There is a highly significant correlation (P < .01) of fruit weight
with bat weight for fruits carried into nets by the three largest species
of bats in the canopy frugivore guild (Fig. 5). Most of the points in this
figure represent Ficus insipida fruits, the most important food species
in the diet of all three bat species. Thus, even though these three bats
have high overlap in food species (Table 5), individuals specialize on
food particles proportional to their body weights. Smaller canopy
frugivore species probably do the same with F. yoponensis which is
quite variable in fruit weight.
Each fig specialist has a distinct temporal cycle of flight activity.
The three largest species, V. caraccioloi, A. jamaicensis, and A.
lituratus, have activity peaks at different times of the night (Fig. 6).
Since these three species frequently feed in the same individual trees in
the course of the night, offsetting activity patterns probably function
TABLE 7.-WET WEIGHTS IN GRAMS OF SOME BAT FRUITS COLLECTED BENEATH
FRUITING TREES ON BCI.
Fruit weights
Plant species Range Mean S.D. N
Ficus insipida 7.1-11.4 9.1 1.5 10
Ficus obtusifolia 14.2-19.0 17.1 2.5 3
Ficus yoponensis 1.5- 5.6 3.1 1.1 12
Anacardium excelsum 4.2- 6.2 5.1 0.7 7
Calophyllum longifolium 9.3-17.7 14.7 3.3 7
Dipteryx panamensis 18.0-26.3 22.3 3.6 5
Spondias radlkoferi 8.6-13.0 10.6 1.4 9
Quararibea asterolepis 4.9- 6.3 5.4 0.6 4
Astrocaryum standleyanum 17.0-20.5 18.8 1.8 4
Piper cordulatum 0.5- 2.0 1.2 0.5 15
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY 375
A Vompyrodes caraccioloi Y= 0.23X -392
* Artibeus jamoacensis r= 0.68
o A. lituratus
S
*
A O
I I ~I I
35 40 45 50
BAT WEIGHT (g)
55 60 65 70
FIGURE 5.-Linear regression of fruit weight on bat body weight for fruits carried into
nets by V. caraccioloi, A. jamaicensis, and A. lituratus.
25- Artibeus jamaicensis N=829
........ A. lituratus N=86
--- Vampyrodes caraccioloi N=38
!! 20-
S15- /
0
I "
I \ '
I I :
z .:
\ I\ I
0 2 4 6 8 10 12
HOURS AFTER SUNSET
FIGURE 6.-Frequency of capture through the night as a measure of flight activity for
three large canopy frugivorous species.
157
i 10-
5-
nI
BULLETIN FLORIDA STATE MUSEUM
to minimize interspecific interference from crowding at resource trees.
This is evident especially when single trees are in fruit near capture
sites where two or more species are found with feces from the same
fruits. Indeed, there were instances when only a few trees of a given
species were in fruit on BCI and all fig specialists were known to be
eating such fruits. Reduced crowding at resource trees presumably is
important in permitting efficient feeding and in making these bats less
obvious to arboreal and aerial predators (Humphrey and Bonaccorso
1978, Morrison in press).
A similar pattern of offsetting major activity peaks should be ex-
pected in the small canopy frugivores, which feed heavily on Ficus
yoponensis and F. popenoaei. Figure 7 shows that V. pusilla is more ac-
tive in the first two hours after sunset, and C. villosum is most active
later in the night. Small sample sizes prevent a similar comparison of
other small fig specialists.
Artibeus phaeotis, the feeding generalist, has a more even distribu-
tion of activity through the night than any other canopy frugivore
(Fig. 7). Many of the fruits eaten by A. phaeotis are not eaten by other
stenodermine bats, and it need not compromise its feeding times to
avoid resource trees crowded with other bat species.
25- Artibeus phaeotus N=132
--- Vampyressa pusilla N=39
........ Chiroderma villosum N=28
! 20-
CL ..... .........
I '
0.1
0, /
o I
LUI
C\
I / .... ,
( I, \ /\
0 2 4 6 8 10 12
HOURS AFTER SUNSET
FIGURE 7.-Frequency of capture through the night as a measure of flight activity for
three small canopy frugivorous species.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
GROUNDSTORY FRUGIVORE GUILD
BODY SIZE.-TwO species, Carollia castanea and C. perspicillata, in
the subfamily Carollinae of the Phyllostomatidae constitute the
groundstory frugivore guild on BCI. These have mean body weights of
12.4 and 17.9 g, thus differing in body weight by a factor of 1.44.
A few Carollia subrufa were captured and banded by R. K. LaVal in
1972 on BCI (pers. comm.). In 1973 and 1974 I recaptured some of
LaVal's banded C. castanea and C. perspicillata, but I have not en-
countered any of the C. subrufa he marked. It is difficult to distinguish
C. perspicillata and C. subrufa by field characters, and it is possible
that I lumped a few individuals of C. subrufa with C. perspicillata
because I was not aware that C. subrufa was present on BCI. I believe
C. subrufa is very rare on BCI, and that lumping a few of them with C.
perspicillata would influence my data negligibly.
FOOD SELECTION.-C. castanea and C. perspicillata are food
generalists eating a fairly even distribution of a large number of kinds
of fruits and have large niche breadth values (Tables 8 and 9). Though
no one food species dominates their diet in any one season, 11 species
of the woody shrub genus Piper (Piperaceae) constitute the bulk of the
diet of C. castanea and nearly one-third of the diet of C. perspicillata. I
identified 10 species of pipers in C. castanea fecal samples and 9
species from those of C. perspicillata. At least one species of piper has
mature fruits in any month on BCI (see Fig. 2). C. castanea and C.
perspicillata eat pipers all year long, but pipers were less important in
the diet of C. perspicillata from mid-September through mid-
November. C. perspicillata appears to feed almost exclusively on sub-
canopy and canopy fruits in the late wet season; particularly impor-
tant is Quararibea asterolepis. Other fruiting trees are important food
species along with pipers at other seasons. Though fruiting shrubs
dominate the diet of C. castanea, fruiting trees are somewhat more im-
portant than shrubs for C. perspicillata.
In addition to fecal samples from captured animals, food habits
data for C. perspicillata were obtained by monitoring droppings below
two day roosts of this species. Both roosts were in hollow Anacardium
excelsum trees. With the exception of fruit from A. excelsum, all com-
mon food items identified from the day roost droppings appeared as
important food items in fecal samples from captured bats during the
same bimonthly periods (Table 10).
Why did the fruit of A. excelsum never show in the fecal material
from captured bats? Probably because Anacardium is the only tree
species that commonly serves as both day roost and food source for C.
perspicillata. These bats need only fly to the canopy of the roost tree,
pick a fruit, and carry it inside the roost to eat it. The bats would
1979
BULLETIN FLORIDA STATE MUSEUM
TABLE 8.-FOOD SPECIES OF C. castanea AND C. perspicillata. NUMBERS INDICATE FECAL
SAMPLES WITH A GIVEN FOOD PRESENT. SAMPLING BEGINS AT MID-MONTH.
Plant species
P. aequale
P. carrilloanum
P. cordulatum
P. marginatum
P. reticulatum
Piper 109
Piper 114
Piper 116
Piper 120
Piper 122
Piper 150
C. castanea
Nov- Mar- Jul-
Mar Jul Nov
Shrubs
9 6
1 1
8 1
4 1 1
2 3
1 1
3
2
C. perspicillata
Nov- Mar- Jul-
Tot. Mar Jul Nov Tot.
10
1 2
4 1
1 1
1
2 1
1 11
3
7 7
1 6
2
1
3
Carludovica palmata
Solanum hayseii
Markea panamensis
Vismia 1
Vismia 2
Brosimum bernadettae
Cecropia exima
Quararibea asterolepsis
Dipteryx panamensis
Cassia undulata
Aechmeia tillandsoides
Trees
1
2
2 11
1 3
1 1
1 7 1
3
Epiphytes
Unknowns
1
1 1
Unknown 104
Unknown 123
Unknown 125
Unknown 127
Insects
TABLE 9.-FEEDING NICHE BREADTHS OF GROUNDSTORY FRUGIVORES. SAMPLE SIZES FOR
CALCULATING NICHE BREADTHS ARE As IN TABLE 8.
Genera of known food plants
Species of known food plants
Percent of diet composed of pipers
Niche breadth (log, B)
C. castanea
8
18
78 (N = 60)
C. perspicillata
10
24
27 (N = 103)
2.63
1
1 9
5
5 9
2
3
2 3
6 6
8
3
4 4
2
6
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
digest and excrete the fruit, usually before flying away from the roost
to forage for other fruits; thus little chance would exist for this pulp to
show up in netted animals. The Carollia colonies in the Anacardium
trees observed consist of 6 to 8 individuals, and each colony probably
had access to more A. excelsum fruits than they could eat.
Anacardium excelsum is the only fruit eaten by bats on BCI that is
not effectively dispersed by them (Dipteryx panamensis though not
dispersed by Artibeus jamicensis is dispersed by A. lituratus.). In the
colonies I observed that Anacardium fruits are carried within the
hollow tree roosts, but even if they are eaten elsewhere, it is the single
large seed, and not the fruit pulp, that is eaten.
There are significant seasonal changes in diet and niche breadths of
both species of Carollia (Table 9). These bats are extreme fruit
generalists in the first half of the wet season. In the dry season and lat-
ter half of the wet season, niche breadths are narrower. C. castanea
feeds almost entirely on pipers during the dry season, but in much of
the wet season Markea panamensis, a tree, is an important dietary
item. Throughout the year pipers constitute 30 to 40 percent of the
food items eaten by C. perspicillata with various trees sequentially
becoming important food sources. Most important are Dipteryx,
Anacardium, and Quararibea in the dry, early wet, and late wet
seasons respectively. Also in the early wet season insects are impor-
tant in the diet of C. perspicillata.
Overlap between the diets of the two Carollia is moderate in terms
of food species. A CX value of 0.585 is obtained from lumping the
dietary data from the year's fecal samples. Food overlap was highest
in the May-July sampling, CX is 0.798. This latter value and the annual
value of overlap would be somewhat smaller if it were possible to cor-
rect for Anacardium eaten in roost trees by C. perspicillata. Even
though roosts were not monitored, it is unlikely that C. castanea eats
much of this fruit, as it is larger than all other important fruits in the
diet of C. castanea and probably too large for efficient handling.
HABITAT SELECTION.-Of the three habitats sampled, the Carol-
linae were most common in the second growth forest and least com-
mon in the mature forest, as are their most important food plants. C.
castanea accounted for 21.7% of all bats captured in second growth
young forest, 2.7% of the bats in creeks, and 1.4% of the bats in
mature forest (Fig. 4). C. perspicillata constituted 15.8%, 16.0%, and
5.4% of the individuals captured in those habitats. Whereas many
species of pipers grew abundantly in the sunlight of the open canopy
second growth and along the creeks (though less so along creeks), only
one species, P. cordulatum, was abundant in the shade of the mature
forest.
BULLETIN FLORIDA STATE MUSEUM
VERTICAL STRATIFICATION.--C. castanea and C. perspicillata were
both captured more frequently at ground level than at upper levels of
the forest (C. castanea = 20 ground level, 14 upper levels; C.
perspicillata = 50 ground level, 34 upper levels), but the difference was
not statistically significant. Both species feed on plants of ground and
canopy levels. Known groundstory fruits make up 78.4% of the diet of
C. castanea and 38.0% of the diet of C. perspicillata. During seasons
when these bats feed mostly on canopy fruits, they are captured more
frequently in high nets and traps.
FEEDING BEHAVIOR.-Carollia castanea and C. perspicillata both
have been captured carrying fruits and presumably use night roosts as
do canopy frugivores. Some fruits are carried back to the day roost for
consumption (Table 10).
Both species of Carollia show major peaks of flight activity in the
first hour of darkness (Fig. 8). This is earlier than the start of most
canopy frugivores' activity and is probably due to the groundstory
becoming dark about an hour before the canopy level of the forest. Pat-
terns of flight activity in groundstory frugivores are bimodal or
trimodal as are those of canopy frugivores.
SCAVENGING (OR JUICER) FRUGIVORE GUILD
BODY SIZE.-Centurio senex (Stenoderminae, Phyllostomatidae),
the wrinkle-faced bat, is the sole member of the scavenging frugivore
guild. A lactating female weighed 22 g, and a pregnant female weighed
27 g. No other weights are available from BCI for this species, nor are
there data on vertical stratification or habitat use.
FEEDING BEHAVIOR.-Goodwin and Greenhall (1961) mentioned
finding fruit pulp in stomachs of C. senex from Trinidad. Of the in-
dividuals that I captured on BCI, one defecated an unidentifiable fruit
TABLE 10.-FREQUENCY OF OCCURRENCE OF FOOD SPECIES OF A COLONY OF Carollia
perspicillata As DETERMINED FROM FRUIT DROPPINGS AND SEEDS BELOW
THE DAY ROOST. SAMPLING PERIODS BEGIN AT MID-MONTH.
Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Total
Anacardium excelsum 5 83 39 127
Piper cordulatum 39 35 9 83
P. reticulatum 6 6
Piper 109 6 6
Solanum hayseii 1 1 2
Vismia 1 2 2 4
Quararibea asterolepsis 5 15 20
Cassia undulata 5 1 6
Unknown 155 12 12
Unknown R-1 3 q
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
pulp and the other carried a fresh Spondias radlkoferi fruit in its
mouth. From several morphological features, particularly the small
teeth and narrow esophagus, Paradiso (1967) concluded that C. senex
probably feeds on a "soft fruit or fluid" diet. Its small teeth and lack of
facial hair suggest that it possibly feeds on very juicy, over-ripe fruit
or decaying fruit. The amount of rotting fruit on the forest floor was in-
credibly large on BCI and potentially could have provided an abun-
dant food resource for such a bat. I have tentatively designated it a
"scavenging frugivore".
An alternative suggestion is that Centurio may feed on very juicy
fruits still clinging to trees. S. R. Humphrey (pers. comm.) believes
from analysis of jaw structure that Centurio is best adapted for
feeding on large, ripe, soft fruits that have very thick pericarps, such
as papayas and mangos.
NECTAR-POLLEN-FRUIT-INSECT OMNIVORE GUILD
BODY SIzE.-The nectar-pollen-fruit-insect omnivore guild
(hereafter called the omnivore guild) contains three species, all of the
25-
\ Carollia castanea N=37
20
S\--- C. perspicillata N=112
UlS
U I I
15- I
S10-\
O I \
I I /
u
C 5- \
0 2 4 6 8 10 12
HOURS AFTER SUNSET
FIGURE 8.-Frequency of capture through the night as a measure of flight activity for
two groundstory frugivorous species.
BULLETIN FLORIDA STATE MUSEUM
family Phyllostomatidae: Glossophaga soricina (Glossophaginae),
Phyllostomus discolor (Phyllostominae), and Phylloderma stenops
(Phyllostominae). Mean body weights for these species are given in
Table 11. The dimorphism in body weights between male and female P.
discolor is significant (P < .05, Student's t-test).
FOOD SELECTION.-Nectar and pollen are consumed by guild
members almost exclusively in the dry season, as large flowers
suitable for bats are in bloom only then (see Phenology). The few data
available suggest that during the wet season fruit and insects become
dietary staples (Table 12). Insects were not present in the food samples
of G. soricina on BCI, probably because of poor sample size and the
fact that this species moved out of the study area during the wet
TABLE 11.-WEIGIITS OF OMNIVOROUS BATS ON BCI. COLUMN HEADINGS AaE DEFINED
IN TABLE 1.
Bat species X S.D. N Wgt/wgt,,
G. soricina 9.8 1.0 9 -
P. discolor 42.2 3.9 27 4.36
males 44.6 3.6 17 -
females 39.7 2.1 10
P. stenops 61.8 1 1.42
TABLE 12.-SEASONAL USE OF POLLEN AND FRUIT BY TIHE OMNIVORE GUILD. NUMBERS
INDICATE POLLEN SWABS AND FECAL SAMPLES COMBINED.
Dry season Wet season
Food species samples samples
P. discolor (N = 23)
Pollen:
Ochroma lagopus 6
Pseudobombax septenatum 6
Unknown 202 1
Fruit:
Cecropia exima 2
Unknown 124 3
Insects: 3
G. soricina (N = 6)
Pollen:
Ochroma lagopus 3
Unknown 201 1
Fruit:
Cecropia exima 1
Piper 109 1
P. stenops (N = 2)
Fruit:
Unknown 110 1
Unknown 151 1
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
season. Howell and Burch (1974) reported that it ate insects. Nothing
beyond Jeanne's (1970) observations of P. stenops eating social wasp
larvae and my two observations of fruit eating is known about the diet
of this bat.
Phyllostomus discolor is neither an extreme specialist nor a
generalist in food species (niche breadth = 1.65). Several types of
flowers are visited for pollen and nectar in the dry season and, in addi-
tion to insects, several types of fruit are eaten in the wet season. The
available data are too limited to consider niche breadth values for P.
stenops and G. soricina.
VERTICAL STRATIFICATION.-All flowers and fruits eaten by P.
discolor and 83 percent of those eaten by G. soricina in this study grow
in the subcanopy and canopy of the forest. Both species were captured
most frequently in upper levels of the forest, 3 of 4 for Glossophaga
and 40 of 54 for Phyllostomus. For P. discolor preference for flying
above groundstory shrubs is highly significant (P < .01, Chi Square
Test).
HABITAT SELECTION.--Phyllostomus discolor was common in the
mature forest and second growth but uncommon over creeks. Some of
the important tree species producing flowers and fruits eaten by
Phyllostomus are common only in second growth (e.g. Ochroma),
others are common only in mature forest (e.g. Pseudobombax), and
still others are common in both habitats (e.g. Cecropia).
FEEDING BEHAVIOR.-During the dry season bats are frequently
captured with pollen heavily dusted over the anterior body. It is likely
that these animals visit numerous flowers in succession, consuming
nectar and performing pollination services at each flower, and later
while roosting ingest pollen by grooming it from the fur and skin.
None of the bats in this guild were captured carrying fruit.
Of the P. discolor captured in all-night samples, 69 percent were
taken within two hours of sunset. Such a strong unimodal pattern of
flight activity (Fig. 9) also is reported by LaVal (1970) and suggested
by Heithaus et al. (1974) for this species in Costa Rica. My data are in-
sufficient for discussing flight activity cycles of Glossophaga, but
LaVal (1970) reported a strong activity peak at dusk and in the first
hour of darkness, just before peak P. discolor activity.
SANGUIVORE GUILD
BODY SIZE.-Of the three extant vampire species, only Desmodus
rotundus, the common vampire, inhabits BCI and surrounding areas.
The mean prefeeding body weight of D. rotundus is 33.5 g.
FOOD SELECTION.-Wild vampires feed only on the blood of
homoiothermic vertebrates (McNab 1973). While vampire feeding
BULLETIN FLORIDA STATE MUSEUM
behavior and prey selection are well documented in agricultural areas
where domestic livestock is the food source (Turner 1975), nothing is
known about prey selection of vampires in areas where only wild
animals are potential hosts.
VERTICAL STRATIFICATION.-Where domestic animals are the
source of food, vampires usually fly within 3 m of ground level (Bonac-
corso, unpubl. data). It is possible that vampires more commonly fly at
the canopy level in forest where no livestock is available, but where ar-
boreal species (e.g. monkeys and birds) may provide sources of blood.
On BCI two vampires were captured in subcanopy nets and one in a
ground net.
HABITAT SELECTION.-Vampires were clearly more abundant on
Buena Vista Peninsula than on BCI. Desmodus was the fourth most
abundant species in the Buena Vista second growth (7.9% of total cap-
tures), whereas on BCI Desmodus was one of the least common species
(0.2% total captures; see Fig. 4). Horses, cattle, pigs, and fowl on scat-
tered farms in the Buena Vista-Frijoles area provide a dependable and
abundant food source that "los vampires" constantly parasitize (Fulo
Sanchez, pers. comm.).
50 -
45
S40
U
S35-
V,
0 30 Phyllostomus discolor N=58
25
0
< -
o 20
L- 10
0-
4 6 8
HOURS AFTER SUNSET
10 12
FIGURE 9.-Frequency of capture through the night as a measure of flight activity for
Phyllostomus discolor.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
GLEANING CARNIVORE GUILD
BODY SIZE.-The largest feeding guild within the bat fauna of BCI,
the gleaning carnivore guild, consists of nine phyllostomine species
which exhibit the largest range in body size in any of the feeding guilds
(Table 13). Micronycteris megalotis, one of the smallest bats on the
island, has a mean body weight of 6.3 g, while Vampyrum spectrum,
the largest species, weighs about 120 g.
FOOD SPECIES SELECTION.-Except for the vertebrate diet of V.
spectrum, guild members feed predominantly on insects; however,
fruits, pollen, arachnids, or lizards supplement the diet of various
species. The collected fecal samples from these species are now being
analyzed and will be published elsewhere.
Novick (1971) hypothesized that large-eared insect- and vertebrate-
eating bats, such as the species in this gleaning carnivore guild, are
adapted to distinguish and capture prey items resting on foliage by
echolocation. Recent information cited below demonstrate that olfac-
tion and sound produced by prey are used by some of these bats to find
prey.
Ross (1967), Wilson (1971b), and Vehrencamp et al. (1977) have
shown that many large-eared bats do feed primarily by gleaning large
insects and birds that nocturnally perch on vegetation or on the
ground. Gardner's (1977) review of the food habits of bats in this guild
further confirms that food items such as lizards and large insects are
gleaned from foliage.
MICRONYCTERIS. Wilson (1971b) reported that large roaches, or-
thopterans, and scarabeid beetles are the most important items in the
diet of M. hirsuta on Orchid Island, a small island adjacent to BCI.
During the dry season fruit became an important component of the
diet of this species as indicated by droppings below the study roost.
My data show that M. megalotis and M. brachyotis also switch in part
TABLE 13.-WEIGHTS IN GRAMS OF GLEANING CARNIVORES. COLUMN HEADINGS ARE
DEFINED IN TABLE 1.
Bat species X S.D. N Wgt/Wgt,~
M. megalotis 6.3 0.6 6 O
M. brachyotis 9.7 1.1 3 1.53
M. crenulatum 14.7 0.7 12 1.52
M. hirsuta 15.2 1.2 7 1.03 (1.57*)
T. cirrhosus 31.0 3.8 13 2.09
T. sylvicola 32.6 3.6 10 1.04
T. bidens 35.6 2.3 7 1.09
P. hastatus 91.2 4.0 7 2.56
V. spectrum 120.0 1 1.31
*Ratio between weights of Al hirsluta and M. hrachyotis.
BULLETIN FLORIDA STATE MUSEUM
to fruit diets in the dry season. M. brachyotis also eats nectar and
pollen. An individual captured in mid-December was thoroughly
dusted with the pollen of a balsa tree (Ochoroma lagopus).
TONATIA. Insect, arachnid (spiders), and lizard fragments were
found in the fecal samples of T. bidens. Insects, arachnids (whipscor-
pions), and plant materials were found in the feces of T. sylvicola on
BCI. A very large male cicada (Fidicina mannifera) that weighed 2.5 g
was carried into a net by a T. bidens in July of 1974. The prothorax of
the dead cicada had been crushed by the bat's teeth. Because this
event occurred in the mating season of the cicadas, during the loud
nocturnal chorusing, it posed the question of how Tonatia locates such
insect prey. Do these bats find such prey via echolocation or by sounds
produced by the insects?
Two T. bidens, one male and one female, were released on separate
occasions into a large outdoor flight cage on BCI. Both individuals
were immediately attracted to calling male cicadas that I held by
forceps inside the cage. The cicadas were plucked from the forceps by
the flying bats and eaten after the bats had roosted. Female cicadas
(which are not capable of singing) held so that their wings could not
move in the forceps were ignored by these bats; however, when the
wings were allowed to flap noisily, the bats again were attracted to the
cicadas and ate them. During later experiments large nocturnal
grasshoppers, katydids, beetles, and moths placed on the inside cage
screening were "gleaned" from the screening and eaten by these bats.
It is obvious that T. bidens was able to locate cicadas from sounds pro-
duced by the cicadas, but whether other large foliage-clinging insects
were echolocated or detected from insect-produced sounds or detected
by some other sensory system remains an interesting question.
PHYLLOSTOMUS. Insects and fruits were found in the fecal samples of
P. hastatus on BCI. It also has been reported by several authors to eat
birds and rodents (Gardner 1977).
VAMPYRUM. V. spectum (the false vampire bat), the largest New
World bat, feeds primarily on birds, rodents, and bats (Vehrencamp et
al. 1977). A hollow roost monitored by Vehrencamp et al. in Costa Rica
had remains of doves, parrots, trogons, cuckoos, anis, and many other
birds weighing between 20 and 150 g. These authors suggested that
Vampyrum locates prey primarily by olfaction, striking animals at
communal roosts with strong odors. D. J. Howell and I kept a Vam-
pyrum alive in captivity for three weeks on a diet of small bats and
birds (10-120 g). When released in a large room with small fruit bats
(10-20 g), the false vampire would fly up behind its flying victim and
slap it into its jaws with a wingtip. One morning at sunrise on BCI, a
false vampire circled about an Artibeus jamaicensis I was untangling
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
from a net. The Vampyrum was apparently attracted by the alarm
calls of the fruit bat and circled for over a minute before leaving.
MIMON. Fecal samples of Mimon crenulatum from BCI contained
insect, arachnid, and lizard remains.
TRACHOPS. Fecal samples of Trachops cirrhosus from BCI contained
insect, whipscorpion, and lizard remains and fruit pulp. Elsewhere this
species is reported to eat lizards, such as anoles and geckos, that are
gleaned from vegetation, as well as fruit and insects (Gardner 1977,
Howell and Burch 1974).
VERTICAL STRATIFICATION. -Mimon crenulatum, Trachops cir-
rhosus, and Tonatia sylvicola show a significant preference for flight in
the groundstory level of the forest, and the small samples for
Micronycteris brachyotis and Tonatia bidens are just below
significance levels for showing a subcanopy-canopy preference (Table
14). Thus the two similarly sized Tonatia species appear to forage in
different vertical strata.
Phyllostomus hastatus and Vampyrum spectrum were captured or
seen flying only in the subcanopy-canopy levels of the forest. The
groundstory (0 to 3 m) on BCI has the densest foliage of the vertical
strata of the forest (E. Leigh, pers. comm.). P. hastatus and V. spec-
trum may be too large to maneuver well through the thick groundstory
vegetation.
HABITAT SELECTION.-Several of the gleaning carnivores prefer
either creek or forest habitats on BCI to the exclusion or near exclu-
sion of the other. Micronycteris brachyotis and Tonatia sylvicola are
both common in the forest but are totally absent from the creek
samples (Fig. 4). Trachops cirrhosus represents 4 percent of all in-
dividuals sampled at creek stations (8th most abundant species in
TABLE 14.-VERTICAL STRATIFICATION OF GLEANING CARNIVORES. YATES CORRECTION
FOR CONTINUITY IS USED ON ALL CHI SQUARE TESTS (SOKAL AND ROHLF
1969).
No. of bats captured at No. of bats captured at
Bat species ground level, 1 to 3 m subcanopy level, 3 to 12 m
M. megalotis 1 3
M. brachyotis 6 12
M. hirsuta 6 3
M. crenulatum 9* 1
T. cirrhosus 14** 0
T. sylvicola 18** 3
T. bidens 2 8
P. hastatus 0 4
V. spectrum + 0 3
*Significant by Chi Square Test (P < .05).
**Highly significant by Chi Square Test (p < .01).
+ Based on two net captures in Costa Rica and one visual sighting on BCI.
1979
BULLETIN FLORIDA STATE MUSEUM
creek samples) but only 0.5 percent of the individuals sampled at
forest stations (17th most abundant species in forest stations). All
other species in the guild are approximately equally abundant in creek
and forest samples. Comparisons with Buena Vista second growth
samples are not made, because most species in this guild were under-
represented at Buena Vista from lack of harp-trapping.
It appears that a spatial mechanism, specialization in foraging
microhabitat, permits Trachops cirrhosus, Tonatia sylvicola, and
Tonatia bidens, all similar-sized gleaning carnivores, to partition food
resources within the same macrohabitat. T. cirrhosus seems to
specialize on prey in low foliage along creeks, T. sylvicola on prey from
groundstory forest foliage, and T. bidens on prey from trees in the
forest and along creeks.
FEEDING BEHAVIOR.-The gleaning carnivores eat rather large
prey items relative to their body weight. It probably is common for
them to carry prey to a night or day roost for consumption (Wilson
1971b, Vehrencamp et al. 1977, pers. observation).
Data on activity cycles are too scant for meaningful analysis. M.
brachyotis, M. crenulatum, T. sylvicola, and T. cirrhosus appear to
have a major peak of flight activity in the first two hours after sunset.
SLOW-FLYING HAWKING INSECTIVORE GUILD
Eight species belonging to three families constitute the slow-flying
hawking insectivore guild. Four species belong to the Emballonuridae,
two to the Vespertilionidae, and two to the Mormoopidae. An addi-
tional species, Thyroptera tricolor (Thyropteridae), is known only from
a single 1973 sighting in recent years on BCI. T. tricolor perhaps
should be included in this guild if a population still exists on BCI;
however, the species is probably near extirpation on the island because
of plant succession that has resulted in the disappearance of most
large-leaved groundstory plants (e.g. Musa and Callithea) used as
roosts (Findley and Wilson 1974).
BODY SIZE.-Mean body weights of species in this guild range from
4.2 to 22.6 g (Table 15). Wing morphology and flight behavior (Bonac-
corso, unpubl. data) suggest that species within the same family are
most similar in foraging behavior. Thus, species are grouped in
subguilds by families.
FOOD SELECTION.-All species of this guild feed largely on small
flying insects. Prey items are eaten on the wing rather than carried to
roosts. Some emballonurids hover around tree foliage and feed to some
extent on insects attracted to host trees (Bradbury and Vehrencamp
1976). One BCI fecal sample from Pteronotus parnellii examined by
Terry Erwin contained leg parts of a small alleculid beetle. All other
samples await species identification.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
TABLE 15.-WEIGHTS OF SLOW-FLYING HAWKING INSECTIVORES. COLUMN HEADINGS ARE
DEFINED IN TABLE 1.
Bat species X S.D. N Wgt/wgt,,,
Emballonuridae
S. leptura* 4.2 1
C. maximiliani* 5.2 1 -
S. bilineata males 7.7 0.56 11 1.47
S. bilineata females 8.7 0.70 3 -
P. kappleri* 11.2 2 1.46
Vespertilionidae
R. tumida 4.2 2 -
M. nigricans 4.4 0.67 11 1.05
Mormoopidae
P. saupurensis 16.5 1 -
P. parnellii 22.6 1.48 30 1.37
*Males and females are probably dimorphic in body weight.
VERTICAL STRATIFICATION.-Pteronotus parnellii usually fly within
3 m of the ground (Table 16). Myotis nigricans and S. bilineata com-
monly fly in groundstory and subcanopy levels of the forest.
Peropteryx kappleri is a specialist on insects of the subcanopy (Brad-
bury and Vehrencamp 1976). This also is indicated by the capture of all
four BCI individuals in high nets, and numerous visual observations I
made in Belize.
HABITAT SELECTION.-P. parnellii is the second most abundant
species in the forest but is very rare over creeks (Fig. 4). The single
specimen of P. suapurensis was captured in forest.
Myotis nigricans was captured only at forest stations, whereas
Rhogeessa tumida was captured only at or near creeks. These two-
similar-sized species thus may differ in habitat requirements.
Visual observations of Saccopteryx bilineata during its crepuscular
foraging indicate that individuals repeatedly fly in circles around
feeding territories in small clearings of the forest (e.g. treefalls) or over
creeks. Frequently I have watched Saccopteryx chase intruding con-
TABLE 16.-VERTICAL STRATIFICATION OF SLOW-FLYING HAWKING INSECTIVORE SPECIES.
No. of bats captured at No. of bats captured at
Bat species ground level, 1 to 3 m subcanopy levels, 3 to 12 m
S. bilineata 7 4
C. maximiliani 2 0
P. kappleri 0 4
R. tumida 1 0
M. nigricans 3 3
P. parnellii 74* 1
*Highly significant by Chi Square Test (P < .01) with Yates Correction for Continuity (Sokal and Rohlf 1969).
1979
389
BULLETIN FLORIDA STATE MUSEUM
specifics out of their territories, emitting high pitched audible sounds
as they fly. Bradbury and Vehrencamp (1977) reported that individual
males defend noctural feeding territories admitting only females that
roost and mate with them.
FLIGHT BEHAVIOR.-Pteronotus parnellii is one of the most com-
monly seen species on BCI as it flies low along forest trails. Ultrasonic
pulses picked up by a bat detector indicate that P. parnellii feeds as it
flies back and forth in long loops along forest trails and groundstory
vegetation.
Flight activity of P. parnellii through the night is bimodal, with a
major activity peak occurring 1 to 4 hours after sunset (Fig. 10). Data
on activity cycles of the other guild members are limited, but P.
parnellii may be the only species that has no peak of activity the first
hour after sunset. Based on netting, visual observations, and
ultrasonic detection, the emballonurids are active from an hour before
sunset to an hour after sunset and again at a similar period around
sunrise.
REPRODUCTION
Three patterns of reproduction occur in Neotropical bats: seasonal
monestry, seasonal polyestry, and year-round polyestry (Fleming
40
35
U
S30- \ Pteronotus parnelli N =194
O 25 -
S20-
I- 0 -
5-
10
0 2 4 6 8 10 12
HOURS AFTER SUNSET
FIGURE 10.-Frequency of capture through the night as a measure of flight activity for
Pteronotus parnellii.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
1973). Present information indicates that a single young is born per lit-
ter, except in the genus Rhogeessa in which the usual litter size is two
(Humphrey and Bonaccorso 1978). Reproductive patterns within bat
species vary with geography and ecological conditions, all data below
refer to BCI except where otherwise stated.
CANOPY FRUGIVORE GUILD
Canopy frugivores are seasonally polestrous, with one birth peak at
the end of the dry-to-wet transition and a second about the middle of
the wet season (Figs. 11-13, Table 17; Wilson 1979). The first birth
peak for all species coincides with the beginning of the first predic-
tably steady rains of the year in late April and May, a time of fruit
abundance. Large species, such as A. jamaicensis and A. lituratus, are
pregnant (as detectable by palpation) by the first week of January.
Small species like A. phaeotus are not in a similar stage of pregnancy
until late January. Lactation then proceeds for 1 or 2 months (during
continued food abundance). There is a postpartum estrus, and females
are well advanced in the second pregnancy of the year while lactation
is still underway (Fleming 1971, this study).
The second birth and lactation peaks are less synchronized among
species because of differences in gestation and lactation periods; the
same is true to a lesser degree within species because of individual
Artibeus lituratus
80- Pregnant R Lactating
70- Nonreproducing
S60-
50-
S40
30-
z
L 20-
10-
few data
J-M M-M M-J S-N N-J
N=23 11 6 17 13
Fli;uiF: 11.-Reproductive timing in female Artibeus lituratus.
1979
BULLETIN FLORIDA STATE MUSEUM
variation. For example, the second peak of lactation occurs in July-
September for A. jamaicensis and A. phaeotis, but not until
September-November for the larger A. lituratus.
All canopy frugivores are reproductively quiescent in the late wet
season. Females of small species appear inactive from October through
December. The two largest species of the guild appear reproductively
inactive from mid-October through December, at least by external
signs, but histological preparations (Fleming 1971) indicate that A.
jamaicensis females are in early stages of pregnancy with drastically
slowed embryonic growth occurring in these months. Whether other
species also pass through a period of delayed development at the end
of the wet season is not known. Nevertheless, the energy channeled in-
to reproduction by canopy frugivores is markedly reduced during the
late wet season, a time of fruit scarcity.
Artibeus jamaicensis
[J Nulliparous T?
0 that have given birth
80-
40 17
20
few data 71
90-
90 iD Pregnant
0- Prnant Nonreproducing
4 80- Lactating
70-
0
60-
0
50-
U 40-
u 0ii~
J-M M-M M-J J-S S-N N-J
N= 58 92 53 59 82 23
FIGURE 12.-Reproductive timing in female Artibeus jamaicensis.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
During the March-May sampling, 27 percent of the A. jamaicensis
adult females captured were nulliparous (Fig. 12,), and nearly all of
these probably had been born in the first or second birth pulse of the
previous year (8 to 12 months before). Through the next three bi-
monthly periods the percentage of nulliparous females in the popula-
tion steadily rose to 49 percent, as recruitment occurred from the off-
spring of the year. Between November and the following March the
proportion of nulliparous females declined, not from their having given
birth, but presumably from higher mortality and/or dispersal rates
than are found in older females.
GROUNDSTORY FRUGIVORE GUILD
Groundstory frugivores follow a reproductive pattern similar to
canopy frugivores. There are two births per year per female, one in the
dry-to-wet season transition and the other in mid-wet season (Fig. 14).
Simultaneous pregnancy and lactation in March-May and recaptures
of marked individuals indicate that females have a postpartum estrus.
Females are reproductively inactive from mid-October through
December.
Artibeus phaeotis
1001 Pregnant
90- j Lactating
80 r Nonreproducing
V)
S-70
60
o 50
O 40
z
U 30
20-
10-
few data
J-M M-M M-J J-S S-N N-D
N=28 14 14 15 19
FIGURE 13.-Reproductive timing in female Artibeus phaeotis.
1979
BULLETIN FLORIDA STATE MUSEUM
SCAVENGING FRUGIVORE GUILD
Though only two female Centurio were captured, one female preg-
nant in February and another lactating in November indicate that the
wrinkle-faced bat is probably seasonally polyestrous like other fruit
bats.
NECTAR-POLLEN-FRUIT-INSECT OMNIVORE GUILD
The only reproductive data available for this guild is for
Phyllostomus discolor, which appears to follow the pattern of seasonal
polyestry explained for frugivorous guilds (Table 17).
SANGUIVORE GUILD
Wimsatt and Trapido (1952) suggested that Desmodus rotundus
females are seasonally polyestrous or polyestrous year round. Turner
(1975) demonstrated that D. rotundus in cattle-raising areas of Dry
Tropical Forest in Costa Rica are pregnant or lactating in all months of
the year, but most pregnancies occur in the wet season. Although only
six female vampires were captured in my study, the appearance of
TABLE. 17.-REPRODUCTIVE TIMING IN FEMALE BATS OF PANAMA.*
Bat species
C. castenea
V. pusilla
C. trinitatum
V. helleri
C. villosum
V. caraccioloi
C. senex
P. discolor
D. rotundus
M. megalotis
M. brachyotis
M. crenulatum
M. hirsuta
T. cirrhosus
T. sylvicola
T. bidens
P. hastatus
C. maximiliani
S. bilineata
P. kappleri
R. tumida
M. nigricans
P. suapurensis
G. soricina
Jan-Mar
308
2 1 0
2 0 0
2 0 0
3 0 0
2 0 0
1 0 0
1 1 2
0 1 1
1 0 2
1 0 0
1 0 4
0 0 1
4 0 4
1 1 0
1 0 0
1 0 1
0 0 1
Mar-May
7 1 3
5 7 2
0 0 1
1 1 1
3 10 0
1 1 1
May-Jul
2 3 1
3 1 2
1 0 1
4 0 0
Jul-Sep Sep-Nov Nov-Jan
8 0 5 0 1 3 0 0 12
302
0 1 0
010
1 0 1
0 2 2
0 2 5 0 0 1 0 1 3
1 0 0 2 0 0
1 2 0
120
0 1 1 1
0 0 2 1
0 0 1 0
0
1 2 3 4
0
1 0 2
0 0 2
1 0 0
0 0 2
0 0 1
0 1 0
1 0 0
*Within each bimonthly period the numbers represent the number of pregnant, lactating, and nonreproductive
females captured. Data for species in the accompanying figures are not duplicated here. Data are from this study
and from bats captured in Panama by Fleming et al 1972.
Vol. 24, No. 4
1979 BONACCORSO: A PANAMANIAN BAT COMMUNITY 395
pregnant females in June, July, and August and a lactating female in
January is consistent with either pattern.
GLEANING CARNIVORE GUILD
The fragmentary data available for this guild suggest a bimodal
pattern of seasonal polyestry for the genera Micronycteris, Trachops,
and Tonatia. The first birth pulse in these genera coincides with the
beginning of the wet season (Table 17, Wilson 1979). A pregnant and
lactating female Tonatia sylvicola captured in March provides the first
evidence that this species has two litters per year and a postpartum
estrus.
Mimon crenulatum has a monestrous reproductive cycle (Table 17).
Pregnancy peaks in the dry-to-wet season transition with lactation
peaking in the early wet season. Mimon are reproductively inactive
from September through December.
Carollia perspicillata
] Nulliparous 79
99 that have given birth
80-
60
40-
2 few data few data few data
N=40
90 -rm
90-1 ]Pregnant
S80 Lactating
Nonreproducing
S70-
90-
60
S60-
,_ 50-
z
U
S40-
30
10 -
0 few data few data
0-I
J-M M-M M-J S-N
N=12 42 7 11
Fl(;tmI. 14.-Reproductive timing in female Carollia perspicillata.
BULLETIN FLORIDA STATE MUSEUM
SLOW-FLYING HAWKING INSECTIVORE GUILD
Female Pteronotus parnellii are monestrous (Fig. 15). Pregnancies
occur from late December through mid-April. Lactation proceeds from
mid-March through late October; however, most young bats are
weaned by mid-July. The percentage of females sucking young in the
May-July sampling indicates that at least 53 percent of the adult
females succeed in raising young to the latter stages of nursing. This
figure is actually larger, because some females already had weaned
young by the end of this sampling period. Unfortunately juvenile P.
parnellii were not distinguished from adults in the field.
During the March-May sampling 16% of the captured females were
nulliparous adults, and these were probably all one-year-olds.
Pteronotus parnellii
] Nulliparous 99
S T? that have given birth
80-
60-
40-
20 few data few data
0
100- [ Pregnant
V 90- Lactating
S80 Nonreproducing
7. 0-
S60
0
Z 50-
L 40
J-M M-M M-J J-S S-N N-J
N=10 52 32 21 19 5
FI(URE: 15.-Reproductive timing in female Pteronotus parnellii.
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
However, in the next sampling period 50% of the females captured
were nulliparous, indicating that young of the year were entering the
flying population (top graph in Fig. 15). In the July-September sample,
65% of the females were nulliparous. The proportion of nulliparous
females then declined to 47% by the next sampling period. Associated
with the fact that only 16% of the females were nulliparous in March,
this pattern suggests a high mortality for females in the latter half of
their first year. Such a pattern has been found in temperate Myotis
(Humphrey and Cope 1976).
DISCUSSION
DIVERSITY AND PHENOLOGY
Maximal diversity in the bat community of BCI occurs from March
through July (Bonaccorso and Humphrey, in prep.), the principal
growing season. During this time rains are frequent yet light and
many plants and insects, having passed through reproductive inactiv-
ity in the dry season, undergo rapid growth and reproduction.
Deciduous trees produce new leaves, and mature fruits increase both
in diversity and biomass. Most of the large orders of insects, including
the Coleoptera, Lepidoptera, and Hymenoptera, explosively increase
in numbers and biomass. In general most of the food resources eaten
by bats, with the exception of nectar and pollen, are abundant during
the March-July period, and many species of bats that move out of the
forest habitat in the late wet season return by March.
Minimal diversity within the bat community occurs in the late wet
season. Fruit is scarce both in kinds of mature fruits and biomass, and
fruit bat species diversity is lowest during this period. The species
diversity of insectivorous bats also reaches a minimum during the late
wet season. Though the actual numbers and biomass of insects are
slightly lower in the dry season, the availability of insects as food for
bats is probably lowest in the late wet season, when frequent rains cur-
tail insect and bat activity.
Communities formed by tropical bats are by far the most complex
assemblages of sympatric mammalian species occurring anywhere in
the world. Much simpler communities of bats are found in temperate
latitudes. For example, Panama supports 104 known species of bats
(Handley 1966), whereas similarly sized South Carolina contains only
14 species, and all of the United States and Canada contain only 39
species (Hall and Kelson 1959). Furthermore, 30 to 50 species of bats
are commonly found coexisting within an area of a few square miles in
Neotropical forests. Why are there so many more species of bats in
tropical regions than are found in temperate regions of similar size?
1979
BULLETIN FLORIDA STATE MUSEUM
What mechanisms permit so many similar species to occupy tropical
forest communities?
Orians (1969) concluded that tropical forests support more bird
species than temperate forests because of two attributes unique to the
tropics. First, many kinds of food items that are ephemeral in
temperate latitudes are available year-round in tropical latitudes (e.g.
fruits and insects). Second, vegetation structure in tropical forests is
much more heterogenous than in temperate forests, thus providing
more microhabits for foraging specialization (e.g. more vertical layers,
bromeliads and lianas).
The great variety of year-round food items and habitat heterogenei-
ty explain to some degree the abundant numbers and kinds of bat
species in the tropics. All Nearctic bats north of 320 N latitude are ful-
ly insectivorous. In Panama 42 species are probably fully insec-
tivorous, but the other 63 species feed on fruit, pollen and nectar, fish,
vertebrates, blood, or some combination of the above. At least 10 in-
sectivore species in Panama feed to some extent by gleaning foliage,
whereas only one bat species in South Carolina does so. A number-of
emballonurids appear to feed much of the time on aerial insects that
are flying around foliage, flowers, or fruits. Several species feed chiefly
on insects found over water or on its surface (Hooper and Brown 1968,
Gardner 1977).
A third factor related to the high species diversity of the tropics is
the great range in food particle sizes. Flowers, fruits, and insects
available to bats all range widely in size. I earlier demonstrated that
large canopy frugivores select fruits in proportion to their body size. It
is worth considering whether such a mechanism is a common means of
partitioning food resources both at intra- and interspecific levels of the
bat community.
Hutchinson (1959), McNab (1971a and b), and May (1973) all
theorized that similar species may avoid competition for food by differ-
ing in body weights by a factor of at least 1.3 (McNab and Hutchinson
use the figure 2.0). Each species thus specializes in food particles pro-
portional to its body weight, an easily measurable indicator of the
linear dimensions of food handling apparatus such as tooth row, gape,
tongue length, etc.
Food size plays an important role in the partitioning of food
resources among similar species in many types of animals (e.g. Dia-
mond 1973, Brown and Liberman 1973) and may be particularly im-
portant for fruit bats because of the behavior of carrying fruits in
flight to feeding roosts. In accordance with Schoener's (1969) theory of
optimal foraging, each bat should attempt to maximize the amount of
food it harvests per unit of time and thus select the largest food par-
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
tides it can efficiently find and handle. The weight that a bat can carry
in flight without seriously impeding maneuverability probably sets
the upper limit on food particle size for these animals. In fact, A.
jamaicensis selects F. insipida fruits that are 1.7 times larger than the
average weight of available fruits (Morrison 1978, this study). The
largest figs are left because they are too heavy for effective flight.
The distribution of mean body weights for each bat species on BCI
by guild is plotted in Figure 16. The species within the groundstory
frugivore, canopy frugivore, and piscivore guilds increase in body
weights by a geometric progression of 1.3 to 1.8, with one exception in
the canopy frugivore guild. The relationship between body size and
food size may also be important as a means of resource partitioning
within other guilds: the two species of Pteronotus differ in mean
weight by a factor of 1.4, the three species of Mycronycteris differ by a
factor of 1.5, the males of the sexually dimorphic emballonurids differ
by a factor of 1.2 to 1.5. Unfortunately adequate data on food particle
selection exists only for the three largest canopy frugivores in this
study and for the emballonurid insect-eaters studied by Bradbury and
Vehrencamp (1976), all of which roughly select food particles in direct
proportion to body weight. However, the circumstantial evidence of
strictly adherable increments in body weight within a guild suggest
that food particle size is an important mechanism of food partitioning
and a selective factor controlling body size within the above mentioned
guilds.
FORAGING AND REPRODUCTIVE STRATEGIES
CANOPY FRUGIVORES
Many fruits preferred by bats have attributes of color, odor, taste,
etc. that reduce their availability to, or preference by, most other kinds
of fruit-eating animals (Humphrey and Bonaccorso 1978). Hence,
many of the competitive interactions any bat species encounters over
fruit resources, either in ecological or recent evolutionary time, are
with other species of bats of its own feeding guild or other individuals
of its own species. However, competition between fruit bats and other
frugivorous animals does occur. Morrison (1978) calculated that black
howler monkeys (Aloutata palliata) and the Jamaican fruit bat (Ar-
tibeus jamaicensis) roughly consume 9% and 7% of the annual BCI fig
crop respectively. The howlers prefer unripened figs (Hladik and
Hladik 1969), while Artibeus and other bats will eat only mature
fruits. Thus, howlers reduce the total fig crop that can become
available to fruit bats. Fruits preferred by canopy frugivore bats seem
to be unimportant food items for birds.
GROUND STORY FRUGIVORES
CANOPY FRUGIVORES
SCAVENGING FRUGIVORES
NECTAR-FRUIT OMNIVORES
SANGUIVORES
GLEANING CARNIVORES
SLOW-FLYING HAWKING
INSECTIVORES
FAST-FLYING HAWKING
INSECTIVORES
PISCIVORES
1* * 2
3 45 6 7 8 9 10
111
12 13 14
16 17 18 19
25 26
** * 27,28,29,30
31 32
33
1;4 I3.Z 1
0 10 20 30 40 O5 60
BODY WEIGHT (g
CO
I-)
FIGURE 16.-Mean body weights of bat species by feeding guilds. (Dashed lines separate members of different families that belong to the
same feeding guilds.) (1) Carollia castanea, (2) C. perspicillata, (3) Vampyressa pusilla, (4) Chiroderma trinitatum, (5) Artibeus phaeotis,
(6) Vampyrops helleri, (7) Chiroderma villosum, (8) Vampyrodes caraccioloi, (9) Artibeus jamaicensis, (10) A. lituratus, (11) Centurio
senex, (12) Glossophaga soricina, (13) Phyllostomus discolor, (14) Phylloderma stenops, (15) Desmodus rotundus, (16) Micronycteris
megalotis, (17) M. brachyotis, (18) Mimon crenulatum, (19) Micronycteris hirsuta, (20) Trachops cirrhosus, (21) Tonatia sylvicola, (22) T
bidens, (23) Phyllostomus hastatus, (24) Vampyrum spectrum, (25) Rhogeessa tumida, (26) Myotis nigricans, (27) Saccopteryx leptura,
(28) Centronycteris maximiliani, (29) Saccopteryx bilineata, (30) Peroptery kappleri, (31) Pteronotus suapurensis, (32) P. parnellii, (33)
Molossus molossus, (34) Noctilio labialis, (35) N. leporinus.
20 21 22 23 2
I
I
BONACCORSO: A PANAMANIAN BAT COMMUNITY
Temporal partitioning of the access to a resource may arise when
the resource is concentrated in a small space. Fruiting trees visited by
canopy frugivores tend to be few or moderate in numbers of in-
dividuals, but very large per individual. Each individual tree produces
thousands of fruits. Temporal differences in flight (and feeding) times
between similar-sized species that feed in the same trees is a means to
avoid behavioral interference between species when the food supply is
abundant in amount but limited in spatial distribution.
The foraging strategies of fruit bats should optimize the intake of
energy with respect to the density, abundance, spatial distribution,
and particle sizes of available bat fruits. Moist forest sites throughout
Central America usually contain 8 to 10 species of canopy frugivores
(pers. obs.). Eight species of stenodermine bats form the canopy
frugivore guild on BCI. These bats feed almost entirely on fruits grow-
ing in the forest canopy on trees, vines, and epiphytes. Individuals of
most of these plants occur at very low densities and in patchy distribu-
tions within the forest. Most canopy trees producing bat fruits are
large enough to feed hundreds of bats per night during their fruiting
periods of about a week. Because a great range in size of preferred
canopy fruits is available, it is possible for many bat species to
specialize in taking food particles of different sizes. Seven species on
BCI are fig specialists that partition figs primarily on the basis of size.
The other species is a generalist with regard to the type of fruit in its
diet.
The fig specialists appear to have large home ranges (about 3 km2
for A. jamaicensis) compared to other bats of similar size, and travel
through much of the home range in a night to obtain widely scattered
food resources (Heithaus et al. 1974, Morrison 1978, Bonaccorso, un-
publ. data). Artibeus phaeotis, the fruit generalist, appears to have a
comparatively small home range for its size, probably because it feeds
on more kinds of fruits and thus is more likely to encounter a suitable
food resource in a smaller area than a specialist.
Frugivorous bats consume their own weight in fruit per night (Mor-
rison 1978), because they appear to have low assimilation efficiencies
and high metabolic rates (McNab 1969). Each bat must make about
eight to a dozen visits to one or a few resource trees per night (Mor-
rison 1978, in press). Each visit involves picking a single fruit and car-
rying it away to a feeding roost where the fruit is ingested. Once a tree
with mature fruits is located an individual bat may return to it
repeatedly for over a week, but some time and energy are spent
scouting for trees that will be in fruit in future days (Morrison 1978).
For at least two weeks during the beginning of the dry season,
when fruits are scarce and bat pollinated flowers are abundant, at least
1979
BULLETIN FLORIDA STATE MUSEUM
three canopy frugivores switch partly to pollen and nectar diets. In
drier forest habitats where suitable flowers are available over a longer
dry season, stenodermine bats feed on nectar and pollen through much
of the dry season (Heithaus et al. 1974).
Adult females of all species in this guild have two litters per year.
Birth pulses are synchronized within populations and coincide with
the two predictable seasonal peaks in fruit abundance. Late term
pregnancy, lactation, and learning processes associated with foraging
by young bats, the events of highest energetic cost in the life cycle of
mammals (Miguela 1969; Studier et al. 1973), occur at times of food
abundance.
GROUNDSTORY FRUGIVORES
Groundstory frugivores specialize in eating fruits that grow on
shrubs, most of which are less than 3 m high. These bats also feed on
some canopy fruits, and in the dry forest areas of Belize (Bonaccorso,
unpubl. data) and Costa Rica (Heithaus et al. 1974) guild members also
feed on nectar and pollen in the long dry season.
Two species in the subfamily Carollinae, Carollia castanea and C.
perspicillata, form the groundstory frugivore guild on BCI. In closed
canopy forest habitat throughout the Neotropical region, this guild
contains fewer species than the canopy frugivore guild. In South
America the other genus in the subfamily Carollinae, Rhinophylla, ap-
pears to fit the groundstory guild (Handley 1967). Some species of the
genus Sturnira (Stenoderminae) also may belong in this guild.
Far fewer shrub species than tree species produce bat-dispersed
fruits in tropical forests of Central America (12 versus 27 known
species on BCI; also see Heithaus et al. 1974). Also, shrubs produce a
much smaller range of fruit sizes than trees. On BCI shrub fruits
preferred by bats range from about 0.2 to 2.0 g, a 10-fold range;
whereas tree fruits range from about 2.0 to 30 g, a 15-fold range.
Finally most shrub fruits are soft berries or catkins, but tree fruits ad-
ditionally may be drupes, monkeypods, and other forms. Because of
the greater variation in kinds, sizes, and shapes of canopy fruits there
are many more ways to specialize on canopy fruits than on ground-
story fruits, hence the larger numbers of species in the canopy
frugivore guild.
Groundstory frugivores have small home ranges in comparison to
large bats that specialize on canopy fruits. This probably occurs
because shrub food species are abundant as individuals and more
uniform in distribution than tree species. Groundstory frugivores
usually must visit a large number of shrubs each night to find suffi-
cient food. Each shrub has only a few small mature fruits available per
Vol. 24, No. 4
BONACCORSO: A PANAMANIAN BAT COMMUNITY
night (especially true of pipers) and a given shrub may be stripped of
fruits by other bats before an individual visits it or between return
trips from the feeding roost. When suitable canopy species are fruiting
they are included in the diet. Fruits are picked from the resource plant
and carried to feeding roosts for eating. Most fruits eaten by these
bats are mature only from one to three consecutive months; thus
groundstory frugivores must frequently change food species and
search images. Some insects are eaten, but it is not clear whether these
are taken with fruits or independently hunted.
The reproductive strategy of the groundstory frugivores on BCI is
similar to that of canopy frugivores.
NECTAR-POLLEN-FRUIT-INSECT OMNIVORES
Moist and wet tropical forests have few large flowers suitable for
bat pollination and feeding, and these are primarily available in the
dry season (late December through March on BCI). Extreme nectar-
pollen specialists among the Microchiroptera are common only in dry
tropical forests and deserts (Humphrey and Bonaccorso 1978). Only
species like Phyllostomus discolor and Glossophaga soricina that
switch to other types of food in the wet season make prolonged use of
dry season flowers in moist forest, though some frugivores occasional-
ly visit flowers.
The mechanisms of resource partitioning among nectarivorous
bats are poorly understood. My data and those of Heithaus et al. (1974)
and Alvarez and Gonzales (1970) indicate almost complete overlap
among bat species in the use of flowers. Flowers do have activity
cycles with respect to nectar production, and it is suggested by
Heithaus et al. that temporal differences in bat activity serve to parti-
tion nectar and pollen among bats. On BCI the foraging activity of P.
discolor is compacted into the twilight and first hours of darkness, pro-
bably as a response to inter- and intraspecific competition over nectar.
The first bats that arrive at a flower each night receive a maximal sup-
ply of nectar and successive visitors receive lesser amounts (Heithaus
et al. 1974).
Both Glossophaga and Phyllostomus feed primarily on nectar and
pollen as long as flowers are available. As the wet season begins,
Phyllostomus switches to fruit and insects, and Cecropia fruits
become particularly important. In the dry forests of Costa Rica where
Cecropia is not a common tree, Phyllostomus disappears after the dry
season flowering and does not reappear until the next flowering season
(Heithaus et al. 1974). I expect that they migrate to and from habitats
that have Cecropia fruits available in the wet season and large flowers
in the dry season.
403
BULLETIN FLORIDA STATE MUSEUM
Glossophaga too switches to fruit in the wet season, and other
authors have found it also eating insects then (Fleming et al. 1972;
Howell and Burch 1974). G. soricina is a rare bat on BCI and becomes
even more rare in the wet season, indicating that it may undergo
seasonal habitat shifts.
The reproductive strategy of P. discolor appears to be similar to
that of the frugivorous bats. Two birth pulses occur each year, the first
of which is toward the end of the peak in flowering and at the begin-
ning of the peak in fruiting. Females eat fruit and insects during both
yearly periods of lactation. This diet may be richer in protein than a
pollen and nectar diet.
GLEANING CARNIVORES
Nearly all gleaning carnivores depend on large insects as a primary
food resource, though a wide range of vertebrates, invertebrates, and
even fruits may supplement the diet. This large feeding guild has a
more complex array of partitioning mechanisms than any other guild
on BCI. Differences in body size, food types, foraging microhabitats,
and possibly activity cycles operate to maintain the ecological
distinctness among these species. Future investigators should con-
sider potential competition between bats and other taxa that prey on
large insects, such as nocturnal spiders, caprimulgid birds, and tree
frogs.
Gleaning carnivores prey upon food items moderately large in rela-
tion to their own body weight just as fruit bats do. Also like fruit bats
they carry prey items to feeding roosts whether the food be large in-
sects (Wilson 1971b) or birds (Vehrencamp et al. 1977). Because of the
high protein content of their diet these bats possibly eat a smaller
weight of food in proportion to their body size and also fewer prey
items per night than do frugivores. Thus, gleaning carnivores should
spend less time and energy transporting food items between foraging
sites and roost sites (and in total foraging time) than do frugivorous
bats. Time budgets based on radiotracking by Vehrencamp et al.
(1977) confirm this hypothesis in the case of Vampyrum spectrum. It
would be interesting to compare guilds in more detail in terms of
searching effort devoted to foraging.
Late in the wet season and in the dry season large insects are
relatively scarce, and some gleaning species change foraging patterns.
Several of the small- and medium-sized species become rare on the
island late in the wet season, but return and eat mixed diets of fruit
and insects through the dry season (Bonaccorso and Humphrey, in
prep.). Micronycteris megalotis and M. brachyotis appear to use this
strategy. Tonatia sylvicola, however, remains all year eating insects
Vol. 24, No. 4
404
BONACCORSO: A PANAMANIAN BAT COMMUNITY
and whipscorpions. Janzen (1973) and Janzen and Schoener (1969)
reported that watersheds are dry season refugia for many insect
groups in tropical forests. Perhaps some individuals or populations of
gleaning carnivores move to riparian habitats off the island during
lean times.
Micronycteris, Tonatia, and Trachops bear two litters per year. The
first pregnancy of the year for these species occurs during relative food
scarcity, but the birth pulse occurs as large insects are becoming abun-
dant. The first lactation and the entire second reproductive cycle occur
within months of food abundance.
The peak in pregnancy for Mimon crenulatum, a monestrous
species, occurs about two months after those of the above gleaning car-
nivores. Thus both pregnancy and lactation occur within the year's
peak of insect abundance. Mimon can time its reproductive activity in
this manner because it does not squeeze two reproductive cycles
within the months of large insect abundance as do the polyestrous
species of the guild.
SLOW-FLYING HAWKING INSECTIVORES
Much less is understood about resource partitioning, foraging
strategy, and reproductive strategy within this guild than in the
guilds discussed above. It is possible that each family placed in this
guild should constitute a distinct guild, but not enough is known to be
certain. A common denominator among all these species is that they
capture small aerial insects and eat them while flying. Some guild
members have individual or group feeding territories. Territorial
defense of foraging areas may serve as the primary means of decreas-
ing intraspacific interference over food. Body size, microhabitat, and
activity cycle differences are likely possibilities as primary
mechanisms that reduce interspecific competition for food within the
hawking insectivores.
Small insects are abundant all year long, although specific insects
fluctuate in abundance (Smythe 1974). These bats do not undergo
shifts in diet type as many other species are forced to do. Foraging ac-
tivity occurs in bimodal periods on nocturnal or crepuscular regimes.
Hundreds of very small food items must be eaten each night requiring
very high capture and feeding rates (Gould 1955) compared to other
bat guilds.
1979
BULLETIN FLORIDA STATE MUSEUM
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Vol. 24, No. 4
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