Demography and Natural History
of the Common Fruit Bat,
Artibeus jamaicensis,
on Barro Colorado Island, Panama
CHARLES O. HANDLEY, JR.,
DON E. WILSON,
and
ALFRED L. GARDNER
EDITORS
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY ? NUMBER 511
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S M I T H S O N I A N C O N T R I B U T I O N S T O Z O O L O G Y ? N U M B E R 5 1 1
Demography and Natural History
of the Common Fruit Bat,
Artibeus jamaicensis,
on Barro Colorado Island, Panama
Charles O. Handley, Jr.,
Don E. Wilson,
and
Alfred L. Gardner
EDITORS
SMITHSONIAN INSTITUTION PRESS
Washington, D.C.
1991
A B S T R A C T
Handley, Charles O., Jr., Don E. Wilson, and Alfred L. Gardner, editors. Demography and
Natural History of the Common Fruit Bat, Artibeus jamaicensis, on Barro Colorado Island,
Panama. Smithsonian Contributions to Zoology, number 511, 173 pages, 69 figures, 62 tables,
1991.?Bats were marked and monitored on Barro Colorado Island, Panama, to study seasonal
and annual variation in distribution, abundance, and natural history from 1975 through 1980.
Data gathered advances our knowledge about flocking; abundance; feeding strategies; social
behavior; species richness; population structure and stability; age and sex ratios; life expectancy
and longevity; nightly, seasonal, and annual movements; synchrony within and between species
in reproductive activity; timing of reproductive cycles; survival and dispersal of recruits;
intra-and inter-specific relationships; and day and night roost selection.
Barro Colorado Island (BCI) harbors large populations of bats that feed on the fruit of canopy
trees, especially figs. These trees are abundant, and the individual asynchrony of their fruiting
rhythms results in a fairly uniform abundance of fruit. When figs are scarce, a variety of other
fruits is available to replace them. This relatively dependable food supply attracts a remarkably
rich guild of bats.
Although we marked all bats caught, we tried to maximize the number of Artibeus
jamaicensis netted, because it is abundant Q-h of the total catch of bats on BCI), easily captured
by conventional means (mist nets set at ground level), and responds well to handling and
marking.
An average Artibeus jamaicensis is a 45 g frugivore that eats roughly its weight in fruit every
night. These bats prefer figs and often seek them out even when other types of fruit they might
eat are far more abundant. They commute several hundred meters to feeding trees on the
average, feeding on fruit from one to four trees each night, and returning to a single fruiting tree
an average of four nights in succession. The bats tend to fly farther when fewer fig trees are
bearing ripe fruit, and they feed from fewer trees, on the average, when the moon is nearly full.
These bats, like their congeners, do not feed in the fruiting tree itself. Instead, they select a fruit
and carry it to a feeding roost typically about 100 m away before eating it. We utilized radio
telemetry to assess feeding rates from the number of "feeding passes"?transits between fruit
tree and feeding roost. Bats are often netted while carrying fruit, revealing their diet. Feces also
reveal dietary information.
Adult female A. jamaicensis live in harems of three to 30 individuals with a single adult male.
On BCI the harem groups roost during the day in hollow trees. There is presumably a large
population of surplus males that roost together with nonadults of both sexes in foliage. Females
commute an average of 600 m from their day roosts to feeding sites, and harem males travel less
than 300 m. Twice a year most females give birth to a single young, once in March or April, and
again in July or August; active gestation averages about 19 weeks. Juveniles are first netted
when they are about ten weeks old, and females usually first bear young in March or April
following their year of birth.
OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is
recorded in the Institution's annual report, Smithsonian Year. SERIES COVER DESIGN: The coral
Montastrea cavernosa (Linnaeus).
Library of Congress Caialoging-in-Publicalion Data
Handley, Charles O. (Charles Overtoil), 1924-
Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panama /
Charles O. Handley, Jr., Don E. Wilson, and Alfred L. Gardner.
p. cm. ? (Smithsonian contributions to zoology, no. 511)
Includes bibliographical references (p. ).
1. Artibeus jamaicensis?Panama?Barro Colorado Island.
I. Wilson, Don E. II. Gardner, Alfred L. III. Tide. IV. Series.
QL1.S54 no. 511 [QL737.C57] 591 s-dc20 [599.4] 91-13449
@ The paper used in this publication meets the minimum requirements of the American
National Standard for Permanence of Paper for Printed Library Materials Z39.48?1984.
Contents
Page
1. INTRODUCTION by Charles O. Handley, Jr., Don E. Wilson, and Alfred L.
Gardner 1
2. PHYSIOLOGY by Eugene H. Studier and Don E. Wilson 9
3. REPRODUCTION IN A CAPTIVE COLONY by Lucinda Keast Taft and Charles
O. Handley, Jr 19
4. REPRODUCTION ON BARRO COLORADO ISLAND by Don E. Wilson,
Charles O. Handley, Jr., and Alfred L. Gardner 43
5. SURVIVAL AND RELATIVE ABUNDANCE by Alfred L. Gardner, Charles O.
Handley, Jr., and Don E. Wilson 53
6. POPULATION ESTIMATES by Egbert G. Leigh, Jr., and Charles O. Handley, Jr. . . 77
7. MOVEMENTS by Charles O. Handley, Jr., Alfred L. Gardner, and Don E.
Wilson 89
8. ROOSTING BEHAVIOR by Douglas W. Morrison and Charles O. Handley, Jr. . . 131
9. FORAGING BEHAVIOR by Charles O. Handley, Jr., and Douglas W. Morrison . . 137
10. FOOD HABITS by Charles O. Handley, Jr., Alfred L. Gardner, and Don E.
Wilson 141
11. DIET AND FOOD SUPPLY by Charles O. Handley, Jr., and Egbert G. Leigh, Jr. . 147
12. APPENDIX: METHODS OF CAPTURING AND MARKING TROPICAL BATS 151
LITERATURE CITED 167
FRONTISPIECE.?Artibeus jamaicensis. Pencil sketch by Nancy Moran, Barro Colorado Island, Panama^ October,
1976.
Demography and Natural History
of the Common Fruit Bat,
Artibeus jamaicensis,
on Barro Colorado Island, Panama
1. Introduction
Charles O. Handley, Jr., Don E. Wilson,
and Alfred L. Gardner
BCI Bat Project
In 1974, Charles Handley was invited to develop a project to
monitor bats as part of the Smithsonian Tropical Research
Institute's (STRI) long-term environmental monitoring pro-
gram on Barro Colorado Island (BCI). The STRI monitoring
program, launched in 1970 and supported by the Smithsonian
Environmental Sciences Program (ESP), sought to monitor a
wide array of biotic and physical environmental components of
the island continuously over a long period of time.
The BCI Bat Project was born under the administrative title:
"Biomass and energetics of selected populations in Panama:
Bats." We wanted to monitor demographic parameters and
natural history of all the bats regularly found on BCI. Based on
our earlier experiences, we thought the fauna might total 40
species of bats. The length of the project was designed to
continue through a generation of bats, however long that might
be. The only clue to possible duration was the report (Wilson
and Tyson, 1970) of a seven-year-old Artibeus jamaicensis on
BCI.
At the outset it was evident that ESP funds were spread over
Charles O. Handley, Jr., and Don E. Wilson, National Museum of
Natural History, Smithsonian Institution, Washington, D.C. 20560.
Alfred L. Gardner, NERC, US. Fish and Wildlife Service, National
Museum of Natural History, Washington, D.C. 20560.
Review Chairman: W. Ronald Heyer, Smithsonian Institution. Three
anonymous reviewers are gratefully acknowledged.
too many projects to be able to support a really meaningful
monitoring project for bats. Clyde Jones, then Director of the
National Fish and Wildlife Laboratory, U.S. Fish and Wildlife
Service, offered to provide both financial and personnel
support, and the Bat Project became a joint venture of the
Smithsonian Institution and the U.S. Fish and Wildlife Service,
with Michael A. Bogan, Alfred L. Gardner, and Don E. Wilson
joining Handley as field crew leaders.
Handley made several trips to BCI in 1975 and 1976 to
become familiar with the island and its bats, as well as to
determine what was feasible and how to organize the project.
On 2 July 1977 a year-round capture and marking program
began. With the help of collaborators and dozens of volunteers,
we took turns manning the field survey on BCI until November
1980 when this phase of the Project was completed. Thereafter,
Handley continued work on BCI on a periodic basis?the fall
of 1981, the fall of 1982, and the 12 months from September
1984 through August 1985?with the support of the Smith-
sonian's ESP, STRI, and National Museum of Natural History
(NMNH). The purpose of the continuing study was to maintain
the pool of marked bats, refine the demographic data, and gain
further information on the biology of the bats, particularly their
responses to food sources.
During the reconnoitering phase at the beginning of the
project we focused much of our attention on developing a
reliable, long-lasting, harmless marking system. We estab-
lished colonies of bats at the National Zoological Park (NZP)
that we used in marking experiments and in establishing
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
standards for describing age and reproductive state. As a result,
we discarded forearm banding, tattooing, and heat branding and
settled on necklacing with stainless steel ball chain. Band-
bearing necklaces were first attached to free-living bats on BCI
on 18 October 1976. By the fall of 1980 we had placed 18,953
necklaces on bats.
The project evolved rapidly. We soon realized that our
resources were not sufficient to monitor simultaneously all
species of bats on BCI in an effective manner. We settled on
studying the bat that had proved to be our principle
catch?Artibeus jamaicensis Leach, the common fruit-eating
bat.
At first we established netting stations at places that, based
on experience elsewhere, "looked good for bats," such as
stream valleys, trails through open forest, and gaps along ridges
* The use of product brand names in this publication is not intended as
an endorsement of the products by the Smithsonian Institution.
where underbrush and other vegetation did not interfere with
the nets or obstruct fly ways. However, it became apparent that
abundance of bats coincided with nearby fruit sources and that
what at first appeared to be complicated distributional patterns
for the island's bats proved to be nothing more that a direct
correlation between foraging activity and the uneven distribu-
tion and availability of fruit. We improved our netting success
by making systematic surveys along the trails on BCI to locate
pellets of fruit pulp dropped by feeding bats and then setting
our nets nearby where they were most likely to catch bats.
We realized early in the project that squeaking bats often
attracted others, and in 1978 we began to use the wooden
Audubon Bird Call as a substitute to attract bats into the nets.
At a good site, an Audubon Bird Call*, an occasional
squeaking bat, and one or two nets could produce enough bats
to keep everyone busy for hours.
In the beginning we sometimes caught only two or three bats
in a night, and we were satisfied with catches of 30 bats. Later,
TABLE 1-1.?Bats recorded on Barro Colorado Island, Gatun Lake, Panama.
Family EMBALLONURIDAE
Rhynchonycteris naso (Wied)
Saccopteryx bllineala (Temminck)
Saccopteryx leptura (Schreber)
Cormura brevirostris (Wagner)
Centronycteris maximiliani (Fischer)
Family NOCTOJONIDAE
Noctilio albiventris Desmarest
Noctilio leporinus Linnaeus
Family MORMOOPIDAB
Pteronotus gymnonotus Wagner
Pteronotus parnellii (Gray)
Family PHYLLOSTOMIDAE
Subfamily PHYLLOSTOMINAE
Micronycteris brachyotis (Dobson)
Mkronycterts hirsuta (Peters)
Micronycteris megalolis (Gray)
Micronycteris nicefori Sanbom
Micronycteris schmidtorum Sanbom
Macrophyllum macropkyllum (Schinz)
Tonatia bidens (Spix)
Tonatia silvicola D'Orbigny
Mimon crenulalum (E. Geoffroy)
Pkyllostomus discolor Wagner
Pkyllostomus haslalus(PMas)
Pkylloderma stenops Peters
Trachops cirrhosus (Spix)
Chrolopterus auritus (Peters)
Vampyrum spectrum (Linnaeus)
Subfamily GLOSSOPHAOINAE
Glossophaga commissar is i Gardner
Glossophaga soricina (Pallas)
Lonchophylla robusta Miller
Subfamily CAROLLINAE
Carollia brevicauda (Schinz)
Carollia castanea H. Allen
Carollia perspicillata (Linnaeus)
Subfamily STURNIRINAE
Sturnira luisi Davis
Subfamily STENODERMATTNAE
Uroderma bilobatum Peters
Uroderma magnirostrum Davis
Platyrrhinus helleri (Peters)
Vampyrodes caraccioli (Thomas)
Vampyressa nymphaea Thomas
Vampyressa pus ilia (Wagner)
Chiroderma villosum Peters
Mesophylla macconnelli Thomas
Artibeus hartii Thomas
Artibeus jamaicensis Leach
Artibeus lituratus (Olfers)
Artibeus phaeotis (Miller)
Artibeus watsoni Thomas
Ametrida centwio Gray
Centurio senex Gray
Subfamily DESMODONTINAE
Desmodus rotundus (E. Geoffroy)
Family THYROPTERTOAE
Thyroptera disci/era (lichtenstein and Peters)
Tkyroptera tricolor Spix
Family VESPERTIUONIDAE
Myotis albescens (E. Geoffroy
Myotis nigricans (Schinz)
Rhogeessa tumida H. Allen
Family MOLOSSIDAE
Tadarida laticaudata (E. Geoffroy)
Molossus bondae J.A. Allen
Molossus coibensis J.A. Allen
Molossus molossus (Pallas)
NUMBER 511
we were disappointed with less than 100 bats per night, and we
logged many nights with catches exceeding 200. Our best catch
came on 25 October 1979 at a giant Ficus dugandii with ripe
fruit where we netted 282 bats in about four hours.
As of 1985, we had found 56 species of bats on BCI (Table
1-1). Bonaccorso (1979) categorized the bats of the island into
nine "feeding guilds." The distribution of the 56 species among
Bonaccorso's guilds is: canopy frugivores (14), groundstory
frugivores (4), scavenging frugivores (2), omnivores (4),
sanguinivores (1), gleaning carnivores (12), slow-flying hawk-
ing insectivores (14), fast-flying hawking insectivores (4), and
piscivores (1). A. jamaicensis, the major subject of this report,
is a canopy frugivore.
By every measure A. jamaicensis is the most widespread and
abundant bat on BCI (Table 1-2). On a yearly basis, it averaged
60% of the total catch of bats, and we caught it almost every
night that nets were set. Altogether, in the period 1975-1980
(including bats captured before marking with necklaces began),
we recorded 17,820 captures of A. jamaicensis.
By the end of 1980, we had learned enough about A.
jamaicensis including its populations, reproduction, move-
ments, foraging, and physiology to justify a pause to
TABLE 1-2.?Measures of abundance of bats captured on BCI during 1979. Bats were netted on 157 nights, and
captures (including both marks and recaptures) totalled 9118 bats. Tabulations are by frequency of capture
(number and percentage of nights caught), number caught (total), catch per species night (total of a species caught
divided by number of nights it was caught), and catch per netting night (total of a species caught divided by total
nights of netting).
Species
Artibeus jamaicensis
Uroderma bilobatum
Artibeus lituratus
Chiroderma villosum
Carollia perspicillata
Vampyrodes caraccioli
Phyllostomus discolor
Artibeus phaeotis
Carollia castanea
Micronycteris hirsuta
Vampyressa pusilla
Vampyressa nymphaea
Pteronotus parnellii
Tonatia silvicola
Tonatia bidens
Artibeus walsoni
Micronycteris megalotis
Glossophaga soricina
Phyllostomus hastatus
Mimon crenulatum
Rhogeessa tumida
Trachops cirrhosus
Cormura brevirostris
Platyrrhinus helleri
Micronycteris brachyotis
Macrophyllum macrophyllum
Micronycteris nicefori
Saccopteryx bilineata
Desmodus rotundus
Glossophaga commissarisi
Myotis nigricans
Micronycteris schmidtorum
Phylloderma stenops
Centurio senex
Vampyrum spectrum
Uroderma magnirostrum
Lonchophylla robusta
Carollia brevicauda
Artibeus hartii
Mean catch
per species
night
36.3
9.2
6.0
4.4
4.0
3.9
3.3
2.2
2.0
1.8
1.8
1.8
1.7
1.6
1.6
1.6
1.6
1.6
1.6
1.5
1.5
1.4
1.4
1.3
1.2
1.2
1.1
1.1
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
1.0
Rank
1
2
3
4
5
6
7
8
9
10
10
10
13
14
14
14
14
14
14
20
20
22
22
24
25
25
27
27
29
29
29
29
29
29
29
29
29
29
29
Total
5484
551
717
172
428
325
130
235
154
91
87
51
86
113
77
67
35
28
26
50
3
70
7
31
13
11
21
8
12
8
7
5
5
3
2
2
1
1
1
Mean catch
per netting
night
34.9
3.5
4.6
1.1
2.7
2.1
0.8
1.5
1.0
0.6
0.6
0.3
0.6
0.7
0.5
0.4
0.2
0.2
0.2
0.3
0.02
0.4
0.05
0.2
0.08
0.07
0.1
0.05
0.08
0.05
0.05
0.03
0.03
0.02
0.01
0.01
0.01
0.01
0.01
Nights caught
N
151
60
120
39
107
83
40
108
78
52
49
28
51
71
49
43
22
17
16
33
2
49
5
23
11
9
19
7
12
8
7
5
5
3
2
2
1
1
1
%
96
38
76
25
68
53
25
69
50
33
31
18
32
45
31
27
14
11
10
21
1
31
3
15
7
6
12
4
8
5
4
3
3
2
1
1
1
1
1
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
summarize the information for publication. Handley, Wilson,
and Gardner shared the manuscript preparation. Fortunately,
Cindy Taft, Gene Studier, Doug Morrison, and Bert Leigh, who
were heavily involved with various aspects of the Bat Project,
joined us in the authorship of several of the sections.
The Environment
Protected by its isolation in Gatun Lake, and by the vigilance
of its caretakers, BCI long has attracted biologists seeking to
understand life in the tropical forest. The island provides an
ideal outdoor laboratory for the curious naturalist. The
long-term protection provided by the Smithsonian Institution
and the Government of Panama, combined with easy access
and excellent working and living conditions, make available a
small, but manageable bit of tropical habitat where intensive
and long-term studies of the ecosystem are practical (Figure
1-1).
Once known as West Hill, which sloped to the Rio Chagres
on the north, and the Rio Gigantito to the east, and bordered by
the Gigante and Pefia Blanca swamps on the south and west,
BCI came into being following completion of Gatun Dam in
1914 and the subsequent flooding that formed Gatun Lake.
However, because Gatun Lake took about four years to fill
(Chapman, 1938) we don't know exactly when West Hill
became separated from the mainland.
The resulting island consists of about 1500 ha (3 x 5 km) and
at its highest point (the Plateau) rises to 137 m above the lake.
The remaining hilltop, which comprises the island, is a broad
and flat basaltic cap covered with red clay soils (for which the
island was named) up to 1 m thick.
About 90% of the yearly rainfall occurs between May and
December, followed by a pronounced dry season extending
from January to April. Rainfall is not spread evenly, and when
it occurs it often pours. The monthly average during the rainy
season is 31 cm, and the yearly average is about 260 cm (Rand
and Rand, 1982). High rates of transpiration from the forest and
evaporation of the surrounding water of Gatun Lake contribute
to a high relative humidity throughout the year.
The vegetation of BCI has been characterized by Foster and
Brokaw (1982) as scmideciduous lowland forest. Some species
of trees lose all of their leaves for a period of months while
others remain evergreen. Although most species lose their
leaves in the dry season, some do so in the rainy season. Just as
BCI is intermediate in the amount of rainfall it receives,
compared with both coasts of Panama, so is the forest of an
intermediate type, containing elements of both the wetter
Caribbean and dryer Pacific slope forests (Foster and Brokaw,
1982).
Although the structure of forests is shaped by substrates and
climate, the forest on BCI, like forests all over the world, has
been reshaped by the activities of human beings. Foster and
Brokaw (1982) suggested that even the older forest on BCI
might have been cleared 300-400 years ago.
The younger forest on BCI has considerably more evidence
of recent human settlements, including some commonly
cultivated trees and an abundance of crockery and bottles.
Much of the younger forest may date from the 1880's when the
French were attempting to build a trans-isthmian canal (Foster
and Brokaw, 1982).
Bananas and other fruits and vegetables were raised in small
patches near the lab clearing up to the 1950's when all
agriculture on the island was stopped. Trees now cover all of
the former cleared land, except around the laboratory buildings
and in a narrow strip between the canal navigational lights on
Miller Ridge.
Methods
We conducted studies at three sites: (1) Mostly we worked
on BCI, where we mist-netted bats on a large scale and gathered
data on their basic demographic and biological variables. (2) To
gain additional information on movements and fidelity, we
netted on nearby islands and on the adjacent mainland, where
forests are younger and prime age fig trees are more abundant
than on BCI. From navigational lights on Buena Vista Island
and on Palenguilla Point ("Pefia Blanca" light) we regularly
trapped the bats of a pair of maternity roosts (referred to in the
text as the "canal marker roosts"). (3) In addition, to gather
baseline data on reproduction and ontogeny and to establish
standards for describing age and reproductive state in the field,
we maintained colonies of bats at the National Zoological Park
in Washington, D.C., from March 1975 through August 1981.
There was no precedent for the Bat Project, so we learned
techniques and developed protocols and standards by trial and
error throughout the life of the project. What we learned might
be useful for reducing start-up time in future projects. Adoption
of similar standards and terminology could make data
comparable among projects, and greatly enhance the value of
the data. For these reasons we have included only a brief
summary of methods in the body of the text, but have provided
a detailed and fully illustrated treatment of methods as an easily
reprintable appendix.
CAPTURING BATS.?Bats were captured in 12 m nylon mist
nets hung between 3 m tubular aluminum poles. We found it
more productive to net in the vicinity of trees bearing ripe fruit
than in sites selected at random. When it was practical we
placed the nets along a trail near a fruiting tree, around the base
of the tree, or on a ridge overlooking the tree. The nets were set
where underbrush would not impede the flight of bats. As far as
was possible, the nets were arranged in a zig-zag pattern with
ends overlapping about one meter, thereby blocking as much of
an underbrush-free area as possible. The standard netting
station contained ten nets.
We stretched the shelf strings of the nets tight (but not as
tight as possible) to minimize tangling of large Artibeus, and
high enough to keep heavy bats entering the lower shelf from
touching the ground. These tactics facilitated the capture of the
NUMBER 511
BARRO COLORADO ISLAND
0 1/2
Kilometers
Contour Interval 4 0 M e t e r s
FIGURE 1-1.?Barro Colorado Island, Gatun Lake, Panama, showing topography and approximate alignment of
trails.
larger bats, but somewhat diminished our chances of catching
smaller species.
We usually netted five nights each week. Normally the
netting sessions began at dusk and ended when the bats quit
flying, regardless of light conditions. Sometimes we closed up
after an hour or two if netting was slow, but occasionally we
netted until dawn. We furled the nets during heavy rains.
The distress calls of particularly vocal bats were useful for
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
attracting other bats into the nets. In the absence of such bats,
the squeaks of an Audubon Bird Call often were effective in
bringing in bats.
For safety of the bats we preferred bare hands throughout the
capture and marking process. Using folded capture bags as
baffles that the bats might bite, we seldom were bitten
ourselves. Everyone handling bats was protected with rabies
vaccine.
We caught bats at 106 netting localities on BCI (plus 15
others on the mainland and other islands), which was far too
many sites for convenient analysis. Consequently, we arbitrar-
ily allocated the 106 localities on BCI to 20 regional groups of
approximately equal area (Figure 13-5), which we refer to as
"locality groups." We netted often where access was easy and
fig trees were common, and locality groups that encompassed
such areas often included many netting localities. In parts of the
island where access was difficult or fig trees were few, a
locality "group" sometimes included only a single netting
locality. Complete details on marking bats and recording data
can be found in the Appendix.
CANAL MARKER ROOSTS.?In the fall of 1977 we examined
all of the land-based navigational lights (used in pairs to orient
ship's pilots on straight "reaches" of the canal) between
Gamboa and Ganin. Many contained maternity colonies of
Phyllostomus hastatus, Saccopteryx bilineata, and Micro-
nycteris hirsuta. Two (on Buena Vista Island and Palenguilla
Point) contained harems of A. jamaicensis. Fortuitously, both
of the Artibeus roosts were near BCI, and were used by bats that
we mist-netted on BCI and on the mainland. We sampled these
roosts at intervals throughout the project, using a plastic
funnel -like trap, with which we always caught most or all of the
bats in a roost. These roosts gave us information on harem
composition, stability, and recruitment and were our best link
between netting sites and roost locations.
THE ZOO BATS.?Studies on the captive bats at the NZP
were indispensable to the field work on BCI. In 1975, we took
Artibeus jamaicensis, A. lituratus, Uroderma bilobatwn,
Glossophaga soricina, Carollia castanea, and C. perspicillata
to the NZP. The Artibeus died in an accident a few months after
we established the colony, but the others survived and were the
subjects of marking experiments that led to our necklacing
technique. In 1978, we established a new colony, consisting
entirely of A. jamaicensis. This colony is described in detail in
Section 3, Reproduction in a Captive Colony.
Acknowledgments
In a project of such long duration it is inevitable that a great
many people have contributed. We are indebted to every one of
them.
From the inception of the project we enjoyed the interest and
support of David Challinor, then Assistant Secretary of the
Smithsonian Institution. Also, we sought help from offices of
the Smithsonian and its bureaus: James Crockett, Rita Jordan,
and Dante Piachesi, (Smithsonian); John Eisenberg and Devra
Kleiman (National Zoological Park); Mercedes Arroyo, Tom
Borges, Gloria Maggiori, and Donald M. Windsor (Smith-
sonian Tropical Research Institute). On BCI, many people
helped in various ways year after year and were among our
greatest benefactors: Pedro Acosta, Mario Bernal, Barbara
Butler Cusatti, Ricardo Cortez, Miguel Estribi, Alberto
Gonzales, Bonifacio de Leon, Egbert and Elizabeth Leigh, A.
Stanley Rand, and Nicholas Smythe.
Michael A. Bogan and Clyde Jones of the U.S. Fish and
Wildlife Service were closely involved with the project in the
early years. Clyde was instrumental in securing funding and
Mike contributed significantly to the field work. Carl Johnson,
Gorgas Memorial Laboratory, helped us through medical
emergencies.
The radio-telemetry and related roosting and foraging
studies were conducted principally by Douglas H. Morrison.
Special thanks are due to Susan Hagen-Morrison for her
assistance. These studies were supported by STRI, Rutgers
University, and the National Geographic Society. We are
grateful to Jackie Belwood and James Fullard for testing bat
calls and providing information on their acoustics. In addition,
Jackie often joined us at capture stations to help with netting.
Eugene H. Studier led our studies of the physiology of A.
jamaicensis and other bats on BCI. Support for these
investigations came from Sigma Xi, the Penrose Fund of the
American Philosophical Society, the Faculty Development
Fund of the University of Michigan-Flint, the Vice-President
for Research of the University of Michigan-Ann Arbor, the
Rackham School of Graduate Studies at the University of
Michigan-Ann Arbor, and the U.S. Fish and Wildlife Service,
as well as the Smithsonian's Environmental Sciences Program.
John Bassett and Douglas Morrison read the section on
physiology and provided many useful and constructive
criticisms. We thank Renee Seeke for typing the original draft
of that section.
We are grateful to Katherine Rails and Tracey Wemer for
capturing bats in Panama and bringing them to Washington,
D.C., to establish our experimental colonies at the National
Zoological Park (NZP). Nathan Gale, Canal Veterinary Office,
advised us on maintenance of the bats and helped us obtain the
necessary permits for their export. At the NZP the bats were
cared for at first by Todd Davis and Devra Kleiman. Later, in
pursuit of a Master of Science degree at George Mason
University, Cindy Taft devoted much of her time, day and
night, for three years to the bats. The Department of Zoological
Research, NZP, through Devra Kleiman, generously provided
facilities, food for the bats, and expert keepers?Peter Beaman,
John Hough, Eugene Maliniak, Larry Newman, and Tex Rowe.
We were assisted in data gathering by Peter Beaman, Linda
Gordon, Laura Grady, Betty Howser, Devra Kleiman, Eugene
Maliniak, Katherine Rails, and Jane Small. Laura Grady was
especially helpful with compiling the data on wing measure-
ments. The Department of Pathology, NZP, provided necrop-
NUMBER 511
sies of bats that died. We appreciate the advice of Carl Ernst,
Devra Kleiman, and Larry Rockwood, who read early drafts of
the section on Reproduction in a Captive Colony. Luther
Brown, Betty Howser, Karl Kranz, and John Wilson provided
encouragement and indispensable help. The Friends of the
National Zoo provided a summer traineeship and a predoctoral
fellowship to Cindy Taft, who also had partial support from a
National Science Foundation grant (DEB 79-05841) to Luther
Brown.
The seemingly endless job of organizing and compiling the
data was done by Jenny Banner, Greg Blair, Sally Hart Carter,
Kristin Day, Carolyn Gamble, Darelyn Handley, Jennifer
Hoffman, Molly Morton Mayfield, John Miles, Penny Nelson,
Anita Przemieniecki, Cynthia Ramotnik, Becca Shad, Pippa
Vanderstar, and Ellen Winchell. Without Peter Kauslick's
programing skills we would have been hard put to analyze the
data.
Claudia Angle prepared the graphics. For critical reading of
the manuscript we are grateful to Thomas H. Fritts, Ronald W.
Heyer, Paul A. Opler, R.W. Thorington, Jr., and anonymous
reviewers. Final stages of manuscript assembly fell to Darelyn
Handley. She did the word-processing, checked literature
citations, collated figures and tables with text, and patiently
coped with updates to produce several "final" drafts of the text
Finally, there were the field crews who endured rabies
inoculations, suffered innumerable bat and all manner of other
bites and stings, survived the ticks and chiggers of BCI, lugged
heavy net poles up and down slippery slopes and over
interminable miles of trails, were seldom comfortable, were
often rained on, and between looking for bats in the daytime
and catching them at night, had little time for sleep or
recreation. Except for the handful of us who are Smithsonian
Institution or Fish and Wildlife Service staff, all of the field
people were volunteers. They and the data compilers were the
real heros of the project. By year, the field crews were as
follows:
1975 (February and March)
Charles and Darelyn Handley, Katherine Rails, and Merlin
Tuttle.
1976 (February and March; October and November)
Edythe Anthony, Michael Bogan, Todd Davis, Charles and
Darelyn Handley, Nancy Moran, Kim Mortensen, and
Don Wilson.
1977-1978 (July 1977 through August 1978)
Barbara and Michael Bogan, Carolyn Gamble, Alfred Gard-
ner, Charles Handley, Peter Kauzmann, Tad Lawrence,
Molly Morton Mayfield, Patricia Mehlhop, David Saha-
gian, Eugene Studier, Tracey Werner, and Kate and Don
Wilson.
1978-1979 (September 1978 through August 1979)
Greg Adler, Barbara and Michael Bogan, Carolyn Gamble,
Alfred Gardner, Charles Handley, Marshall Hasbrouk,
Douglas and Susan Morrison, Marion and Vern Read,
Lucinda Taft, Merlin Tuttle, and Don Wilson.
1979-1980 (September 1979 to June 1980)
Michael Bogan, Dale Clayton, Adele Conover, Robert Fisher,
Alfred Gardner, Linda Gordon, Charles and Darelyn
Handley, Molly Morton Mayfield, Deborah Page, Char-
les Rupprecht, Norman Scott, Eugene Studier, and Don
Wilson.
1980 (August to October)
Charles Handley, Hui Purdy, and Becca Schad.

2. Physiology
Eugene H. Studier and Don E. Wilson
Although most of our work on Barro Colorado Island (BCI)
was dedicated to marking and recapturing large numbers of
Artibeus jamaicensis, we continually faced questions regarding
the animal's physiology. As our data on population dynamics,
movements, reproductive cycle, and other natural history
variables increased, we needed answers to our physiological
questions. Clearly, the issues of energy, water, and mineral
budgets are critical to understanding factors limiting the bat's
populations. Thus, we conducted physiological studies on
newly captured animals in the laboratories available on BCI.
Most involved nutritional economy as it relates to feeding
behavior, thermoregulation, metabolism, and other mainte-
nance variables.
Energy Balance
FEEDING BEHAVIOR.?Although A. jamaicensis consumes a
variety of foods (Gardner, 1977), the fruits of figs are at the
fore. On BCI, where Ficus insipida and F. yoponensis are
unusually abundant, F. insipida is the fig of choice (Morrison,
1978a); in the Llanos of Venezuela it is F. trigonata (August,
1981).
A. jamaicensis extracts juices of the fruit of these figs
(Morrison, 1980b; Studier, Boyd et al., 1983). The bat bites off
a chunk of pulp and skin and rolls it back and forth with its
tongue against its heavily corrugated hard palate. Juice is
extracted by chewing and by squeezing the shredded pulp
against the hard palate with the tongue. Juices are swallowed
and the shredded pulp is dropped as a "dry" pellet. These bats
are highly efficient at extracting juice from pulp. The technique
of sucking dry one small bite at a time extracted almost as much
juice (91%) as Morrison (1980b) was able to obtain with a
C-clamp press.
Fruits of F. insipida carried into mist nets by A. jamaicensis
on BCI had an average wet mass of 7.0 g (see Section 11, Diet
and Food Supply). However, note that fruit weighed by
Eugene H. Studier, Department of Biology, University of Michigan?
Flint, Flint, Michigan 48503.
Don E. Wilson, National Museum of Natural History, Smithsonian
Institution, Washington, DC. 20560.
Bonaccorso (1975) averaged 9.5 g. Variation in fruit mass from
tree to tree, from season to season, or from year to year may
account for this discrepancy. When humans sense that these
figs are ripe, their average wet mass is 0.58 times less than
when bats select them (Morrison, 1978d). In other words, bats
consider figs ripe at a later stage than humans do. This fact is
important in interpreting results of studies on energetics,
feeding physiology, and fruit composition because there are
marked rapid changes in the composition and concentrations of
nutrients during terminal ripening in fruit (Hulme, 1970). We
know the composition and concentrations of many of the
nutritionally important components of the fruit of F. insipida
(Hladik et al., 1971; Morrison, 1980b; Nagy and Milton, 1979;
Studier, Boyd et al., 1983). Analysis of the juice of this fig is
pertinent to understanding nutritional balance in A. jamaicen-
sis.
The digestive ability of A. jamaicensis is comparable to that
of other nonruminant mammals, at least when it is feeding on
F. insipida (Morrison, 1980b). In this case the bat exhibits an
overall digestive efficiency of 25%-30% of whole fruit
calories. However, such efficiency is misleading because 57%
of the metabolizable energy is dropped as pellets and never
swallowed. Sixty-four per cent of potential energy in food
actually swallowed is assimilated. This value is slightly lower
than assimilation efficiencies of other mammals on low-fiber
diets (Maynard and Loosli, 1969) and may correlate with the
extremely rapid transit time through the bat's digestive tract.
The passage of 25%-33% of swallowed energy as undigested
seeds also contributes significantly to the lowered assimilation
efficiency. On the other hand, 93% of swallowed soluble
carbohydrates are absorbed (Morrison, 1980b), and these
carbohydrates account for almost all retained calories in A.
jamaicensis.
THERMOREGULATION.?We studied thermoregulation in
many species of bats on BCI, but particularly in A. jamaicensis.
We found this bat to be a heterothermic endotherm when we
measured body temperature (Tb) as a function of ambient
temperature (Ta) within 12 hours of capture (Studier and
Wilson, 1970). We determined a relation between Tb and Ta
expressed by
Tb = 8.8 + 0.933 Ta
10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
in a T, range of 8.0?-33.2?C. The regression coefficient for this
relationship (0.933; SE = 0.202) does not differ significantly
from 1.0 and we conclude that in A. jamaicensis, Tb parallels
Ta. Individual bats maintain a constant range of Tb 6.6?-8.3?C
higher than T, throughout the tested T, range.
Previously, Morrison and McNab (1967) reported little daily
fluctuation in Tb cycles in captive A. jamaicensis at an
estimated T, of 27?C. During daylight, some of their data points
(13/128 = 10.1%) were significantly lower than average. They
demonstrated that A. jamaicensis exhibited the thermoregula-
tory pattern of a homeothermic endotherm throughout a T,
exposure range of 5?-39?C. McNab (1969) obtained similar
results in captive A. jamaicensis held for up to two weeks
before testing; no bats had reduced Tb relative to their mean
temperatures.
We reinvestigated these contradictory results and concluded
that although differences in thermoregulatory patterns might
have been related to genetic differences in the populations
studied, more likely the variation reflected different methodo-
logical approaches (Studier and Wilson, 1979). The primary
significance of our 1979 study was the demonstration of a
transition from a heterothermic pattern of Tb regulation on the
day of capture to a homeothermic pattern after three days of
captivity. Such a "captivity effect" for A. jamaicensis may help
to resolve apparently conflicting thermoregulatory patterns in
other mammals, for example, Myotis lucifugus (Stones and
Wiebers, 1967; Studier and O'Farrell, 1972) and Peromyscus
leucopus (Gaertner et al., 1973; Hill, 1977).
Although the captivity effect explains divergent data on
thermoregulation, it does not show which data represent the
natural thermoregulatory pattern. Studier and O'Farrell (1972)
found that the Tb of Myotis lucifugus and M. thysanodes in their
natural roosting sites was highly variable and similar to the data
for newly caught, laboratory-tested individuals. Apparently,
data from bats tested soon after capture better reflect natural
thermoregulatory performance, whereas data from captive bats
held longer reflect their greatest homeothermic capabilities.
We did not attempt to determine which components of the
captivity effect are responsible, either singly or in combination,
for the changeover in thermoregulatory performance, but
several possibilities exist. The increased homeothermic re-
sponse probably does not result from thermal acclimation. We
did not try to hold captive bats at constant T,. Instead, T, for
captive bats fluctuated in slightly muted fashion with that of
BCI's natural environment (Studier and Wilson, 1970).
Furthermore, the captivity effect does not seem to be a general
stress response because stress would be greatest during the
initial hours of captivity; thus bats would be expected to exhibit
the most rigid homeothermy in day zero testing. The captivity
effect may result from individual or combined actions of
reduced activity while caged or the continual presence of
excess food, which the bats can eat at will.
In its natural environment, A. jamaicensis is probably a
homeothermic endotherm during periods of feeding and flight
activity, but loosens Tb control (becoming a nonhomeothermic
endotherm) during roosting (nonfeeding and nonflying epi-
sodes). The slight reduction in Tb at such times would conserve
large amounts of energy (Studier, 1981). Heterothermy in A.
jamaicensis conserves 38.7% and 67.4% of the energy that
would be required of homeothermic individuals at ambient
temperatures of 30?C and 25?C, respectively (Studier and
Wilson, 1970). This would amount to a major energy cost
reduction during a roosting period. We assume that the slight
Tb reduction in A. jamaicensis (Tb of 35.2?C at Ta of 30?C and
Tb of 32.5?C at Ta of 25?C) would not reduce responsiveness to
environmental stimuli during roosting nor would it preclude
initiation of flight.
Thermoregulation probably is dependent on nutritional state
in captive bats. In the wild, A. jamaicensis feeds on fruit that
varies seasonally from scarce to plentiful. Individual bats may
undergo a natural period of diel torpor, whereas captive animals
with unlimited food may never become torpid as long as their
food supply is constant and plentiful. Captive bats routinely
weigh more than wild-caught individuals (see Section 3,
Reproduction in a Captive Colony).
The significant questions regarding possible effect of
nutrition on the variability of Tb in A. jamaicensis are: Does the
heterothermic pattern of bats tested immediately after capture
reflect undernourished individuals? Or, is the homeothermic
pattern of bats kept in captivity a response to overnourishment
and inactivity? Undernourished or not, poor Tb regulation in
newly caught A. jamaicensis is not related to physiological
competence, but reflects reduced metabolic heat production
and rate of depletion of energy stores. Manakins, which are
small frugivorous birds, also exhibit heterothermy on BCI
(Bartholomew et al., 1983).
McNab (1969) reported a resting metabolic rate of 1.70
cc/g/hr for A. jamaicensis within its thermal neutral zone (TNZ)
and a thermal conductance of 0.17 cc/g/hr/?C (below its TNZ).
As with other frugivorous bats, this mass-specific standard
metabolic rate is slightly higher than would be predicted by
Kleiber's (1932) classic relation between metabolism and mass
in mammals. The energetic cost of high Tb homeothermy in A.
jamaicensis is, therefore, higher than expected for a mammal of
its size.
McNab (1983) presented extensive arguments concerning
energetics, body sizes, and the limits to endothermy that can be
expressed by a minimum boundary curve for high Tb
homeothermy. This curve estimates the smallest mass at which
continuous endothermy can occur for a given metabolic rate.
When this minimum boundary curve is drawn by relating the Tb
to Ta differential as a function of body mass, data for A.
jamaicensis falls almost exactly on the curve (McNab, 1982).
A. jamaicensis, therefore, would be predicted to be marginally
able to maintain its reported high homeothermic Tb to Ta
differential. It is, therefore, not surprising that undernourished
(or normally nourished) bats tested immediately after capture
maintain a markedly lower Tb and, consequently, lower Tb to T t
NUMBER 511 11
differentials. As stated previously, the slight Tb reduction found
in A. jamaicensis saves 38.7%-67.4% of the energy required
for maintenance of higher Tb. Such energy conservation would
seem critically important in a species such as A. jamaicensis
that has severely limited reserves of stored energy.
BODY FAT.?Total body fat is a direct indication of overall
nutritional status in vertebrates. Annual variability in body fat
content in numerous Neotropical bats, including A. jamaicen-
sis, has been reported (McNab, 1976; 1982). However,
Neotropical frugivores and nectarivores demonstrate less of the
seasonal variation and none of the gender-related differences
that characterize temperate zone insectivores. All Neotropical
bats exhibit low peak fat reserve levels when compared with
temperate zone bats (Baker et al., 1968; Ewing et al., 1970;
Pagels, 1975; Weber and Findley, 1970). The extremely low fat
reserves reported by McNab (1976) for A. jamaicensis
emphasize its need to reduce daily energy expenditures. Lack
of fat reserves and high intake of dietary carbohydrate suggest
that glycogen should be examined as the normal energy reserve
of A. jamaicensis.
Glycogen levels have not been reported for A. jamaicensis,
but comparable data are available from megachiropterans that,
although not related to A. jamaicensis, are nutritional equiva-
lents. Daily variation in glycogen and fat levels in liver and
flight muscle tissue in Eidolon helvum, a Paleotropical
frugivorous bat, have been reported by Okon et al. (1978).
Their findings show that liver glycogen levels at sunrise (90.0
mg/g) are extremely high in comparison with levels seen in
large domesticated mammals (Watt and Merrill, 1963). Liver
glycogen then drops precipitously in E. helvum until sunset
when levels (35.0 mg/g) reach a range normal for large
mammals. Breast muscle glycogen in this bat remains low
(6.0-8.1 mg/g) and constant throughout the roosting period.
The extreme drop in liver glycogen suggests that glycogen (as
glucose) is the primary energy source of E. helvum throughout
its roosting period. Fat concentrations in liver and breast
muscle in E. helvum show slight increases at sunset, but the
range of all values (5.0-10.3 mg/100 g) is nearly two orders of
magnitude less than fat levels in liver and muscle in other
mammals, large and small (Kirkham and Allfrey, 1972; Watt
and Merrill, 1963). These glycogen levels reflect the high
carbohydrate, low lipid composition of the diet of these bats.
Van der Westhuyzen's (1978) report on another Paleotropi-
cal fruit bat, Rousettus aegyptiacus, provides additional support
for the extreme importance of glucose or glycogen and the
relative unimportance of fat as an energy source in tropical
frugivorous bats. He reported the diurnal cycle of several
metabolites including glucose, free fatty acids, lactic acid, and
pyruvic acid in captive bats during normal feeding cycles as
well as after a "prolonged" fast. The most salient features of
this study are the cycles of blood glucose and free fatty acid
levels. He found that blood glucose levels follow the expected
pattern and fall within normal concentrations for mammals in
general. Most of the bats studied died during 31-32 hour fasts;
however, bats that survived showed no further change in blood
glucose level at 35.3 mg/100 ml. The diurnal pattern of free
fatty acid (FFA) plasma levels follows the expected general
inverse relation to blood glucose levels. Nighttime FFA's are
essentially constant at about 0.5 milliequivalents/liter (mEq/L),
which is quite normal for mammals. If food is withheld for
three hours after sunset, plasma FFA concentrations rise to 4.0
mEq/L concomitant with the fall in blood glucose level.
Although histochemical studies of the muscles of bats
(Armstrong et al., 1977; Talesara and Kumar, 1974) demon-
strate the relative importance of fats and glucose as energy
substrates, muscle enzyme profile studies such as those of
Muller and Baldwin (1978) and, especially, those of Yacoe et
al. (1982), are particularly germane to the present discussion.
Yacoe et al. (1982) determined enzyme activity levels for
citrate synthetase, hexokinase, 3-hydroxyacyl-CoA dehydroge-
nase (HOAD), and phosphorylase in two frugivorous species
(one of which was Artibeus lituratus) and eight insectivorous
species of bats. The four enzymes measured are indirect
indicators (in sequence) of citric acid cycle capacity, blood
glucose oxidation capacity, beta-oxidative capacity, and glyco-
genolytic capacity.
As expected, citrate synthetase activity was extremely high,
among the highest reported for mammalian skeletal muscle,
and there were no interspecific differences. Elevated HOAD
activity levels in all species indicated the expected high
capacity for fatty acid oxidation. Enzymes participating in
glucose storage, mobilization, and cell entry, however, pro-
vided the most intriguing picture. Hexokinase activity in the
frugivorous species was from two to three times higher than in
the insectivorous species. Phosphorylase activity in all species
was on the high end of the normal mammalian range, and,
although not statistically significant, phosphorylase activity in
A. lituratus was higher than in any other species tested.
Frugivorous bats, therefore, retain the capability of rapidly
metabolizing fats as a fuel source but also have unusually high
glycogenolytic ability. The combination of high aerobic and
high glycogenolytic activities previously has been thought to
be mutually exclusive in mammalian muscle fiber (Burleigh
and Schimke, 1969). Such a combination defies easy classifica-
tion in the slow (I) and fast (IIA) and fast (IIB) categories for
mammalian muscle fiber types (Lamb, 1984). Although similar
results have been reported for Australian bats (Muller and
Baldwin, 1978), extremely high capacities for aerobic glucose
oxidation have been reported primarily in flight muscle of
insects, which have a normal diet with high glucose density
(Beenakkers, 1969; Beenakkers et al., 1975; Heinrich, 1979).
Because of its presumed high dietary glucose density and
extremely high glucose assimilation efficiency (Morrison,
1980b), A. jamaicensis, along with other frugivores and
nectarivores, should have much more glucose available for
oxidation than do bats of other dietary preferences. However,
there is a significant energy penalty for converting dietary
carbohydrate to fat (Martin and Lieb, 1979).
12 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
From the foregoing, it may be presumed that A. jamaicensis
produces little fat from glucose and does not take advantage of
the reduced weight and high caloric density gained by storing
energy as fat. Furthermore, A. jamaicensis must exhibit an
extreme facility in the storage, mobilization, and turnover of
glycogen. Finally, the overall energy reservoir in A. jamaicen-
sis is severely limited. In their natural environment, these bats
maintain no significant positive daily energy balance that
would allow for storage of surplus caloric energy.
SALIVATION.?Like many frugivores, A. jamaicensis has
exceptionally large salivary glands (Phillips et al., 1977).
Results of our histological examination of these glands in A.
jamaicensis (Studier, Boyd et al., 1983) are in agreement with
those of Wimsatt (1956). In spite of the large size of the glands
there is no relative increase in number of ducts, nor is there
evidence of relative excess production of serous secretion. The
functional significance of these structural observations include
possible increases in salivary amylase production, increased
involvement in regulation of mineral and water balance, and
overall increase in production of saliva, all related to the
unusually large size of the glands.
Salivary components may act chemically to neutralize
alkaloids in figs. Mucus may hold together the pellets that are
dropped during feeding (Dalquest et al., 1952). We have
suggested that the abundant saliva may strongly buffer gastric
secretions, thus preventing gastric contents from becoming
acidic, while simultaneously coating the gastric epithelium
with an extensive buffering barrier (Studier, Boyd et al., 1983).
If gastric fluid remains above pH 4, salivary amylase should
continue to function. This may be of considerable importance
in view of the rapid passage time and consequent brief
digestion exhibited by A. jamaicensis (Morrison, 1980b;
Studier, Boyd et al., 1983).
The gastric glands in the stomach and duodenum of many
frugivorous bats contain typical parietal and zymogen cells
(Bhide, 1980; Forman, 1972; Rouk and Glass, 1970). Brun-
ner's glands are reduced or absent in frugivorous bats,
including species of Artibeus. The function of Brunner's glands
among mammals is still debated, but for a long time a
connection with protection of the duodenum from damage by
highly acidic chyme leaving the stomach has been suspected. If
saliva of A. jamaicensis has sufficient buffering capacity to
prevent chyme from becoming highly acidic, reduction or
absence of Brunner's glands in these frugivores would be
compensated. Salivary bicarbonate concentration has been
shown to Be directly proportional to the rate of saliva formation
(Burgen and Emmelin, 1961). Because the bicarbonate buffer
system accounts for the bulk of the buffering power of the
saliva (Izutsu, 1981), increased or high relative rates of saliva
production may indicate elevated salivary buffering capacity in
A. jamaicensis. For further discussion of this possibility and for
details of gastric ultrastructure see Phillips et al. (1984).
Caloric Balance
Total daily energy requirements can be estimated by various
methods (Kunz and Nagy, 1988). Maintenance energy (ME)
requirements are most simply calculated as a function of body
mass (W). For endothermic mammals, which maintain constant
high Tb, ME (Kcal/day) = 106 W0-75, where W is in kilograms
(National Research Council, 1978). For an A. jamaicensis
weighing 45 g, estimated ME equals 10.3 Kcal (43.3 Kj)/day
(Table 2-1). Daily energy requirements for an A. jamaicensis
weighing 45 g also can be estimated based on time partitioning
(Table 2-1). The first estimate is based on Morrison's (1978d)
data, in which he partitioned flight time into various activities
and flight distances. Metabolic cost of flight was based on the
wind tunnel studies of Thomas (1975) on other frugivorous
bats where metabolic cost of horizontal flight for a 45 g bat is
0.30 Kj. At an average flight speed of 5 m/sec, the cost of flying
100 m is 0.092 Kj. Appropriate increases in the energy cost of
flight for transport of figs to feeding roosts also are included
(Morrison, 1978d). These flight costs are added to energy needs
for maintaining the basal metabolic rate.
Using data from McNab (1969) for well- or overfed A.
jamaicensis (1.7 cc/g/h), we estimated a basal energy cost of
TABLE 2-1.?Daily energy expenditures for a 45 g Artibeus jamaicensis. All
values are Kcal/days; equivalent Kj/day are given in parentheses. See text for
further details.
Parameters
Based on mass*
Based on time partitioning
Flight costs'"
searching
commuting
between feeding passes
feeding passes
transmitter e
subtotal
Basal metabolism (well- or overfed)'1
Total**1
Basal metabolism (normally- or underfed)8
Total1"'
Based on time partitioning
Flight costsf
Basal metabolism (well- or overfed)d
Totals
Basal metabolism (normally- or underfed)*
Totalf4?
Kcal/day
10.30
0.20
0.28
0.19
1.04
0.11
1.82
8.77
10.59
3.87
5.69
3.20
8.77
11.97
3.87
7.07
Kj/day
(43.30)
(0.84)
(1.17)
(0.79)
(4.33)
(0.50)
(7.63)
(36.70)
(44.33)
(16.20)
(23.83)
(13.40)
(36.70)
(50.10)
(16.20)
(29.60)
? National Research Council, 1978.
b
 Morrison, 1978d.
c
 Additional 1% increment as cost of carrying transmitter in flight.
d
 McNab, 1969.
e
 Studier and Wilson, 1979.
'Morrison, 1980b.
NUMBER 511 13
8.77 Kcal/day. Using metabolic rates of underfed (= normally
fed) A. jamaicensis (0.75 cc/g/h; Studier and Wilson, 1979),
reduces basal energy cost to 3.87 Kcal/day. In either
circumstance, daily energy cost of basal metabolism represents
the major fraction (67.9%-82.7%) of total daily energy
requirements. An additional time-partitioning energy budget
(Morrison, 1980b) is based simply on a minimum estimated
flight time of 45 min/day (Table 2-1). Although this second
time-partitioning budget markedly increases metabolic energy
expenditure for flight (from 1.8 to 3.2 Kcal/day), basal
metabolic costs still represent the major fraction (54.8%-
73.1%) of total daily energy budgets. Kunz (1980) proposed a
daily energy budget for bats in general in which caloric needs
(in Kcal/day) equal 0.92m0-767 (where m is mass in grams).
Kunz's (1980) estimate of daily energy needs, however,
includes data from lactating and pregnant bats as well as from
reproductively inactive individuals. Therefore, he overesti-
mated caloric needs.
The estimates for total daily energy costs to a reproductively
inactive, endothermic A. jamaicensis, maintaining a high Tb are
remarkably consistent with a total range of 10.3-12.0 Kcal/day
(43.3-50.1 Kj/day) and probably represent realistic estimates
for a bat that remains constantly homeothermic. The minimal
daily energy budget of 5.7 Kcal/day (23.8 Kj/day) for
heterothermic individuals is surely an underestimate because
the bats are not continuously heterothermic. The marked
reduction in daily energy demand associated with heteroth-
ermy, however, may be invaluable to free-flying individuals
that have a marginal energy intake. Fleming (1988) estimated
daily energy budgets of 41.9-47.3 Kj/day for Carollia
perspicillata, a smaller phyllostomid with a more varied diet
and different foraging strategy. The similarity between these
figures is striking.
A. jamaicensis extracts 55.5 g of juice per 100 g of fresh fruit
of F. insipida (Morrison, 1980b). Morrison reported that juice
from these ripe figs contained 0.315 Kcal/g; we found 0.415
Kcal/ml (Studier, Boyd et al., 1983). The specific gravity of an
artificial fig juice solution (111 mg glucose per ml) is 1.042
g/cc. Most of the energy in fig juice is in dissolved glucose and
the energy assimilation efficiency of fig juice by A. jamaicensis
is 98.3% (Morrison, 1980b). Using the maximum estimate for
a daily energy budget of 12.0 Kcal/day, an A. jamaicensis
weighing 45 g would need to assimilate all the energy from
28.9 to 36.5 ml of fig juice. Given the 98.3% assimilation
efficiency, this would require 29.4-37.2 ml of ingested fruit
pulp juice or 55.1-69.8 g of fresh ripe fruit. At 7 g per fruit, an
A. jamaicensis would require 8-10 whole fruits of F. insipida
per day to meet its caloric requirement entirely from the
ingestion of the fruits of figs. If average-weight ripe fruits
weighing 5.6 g (Morrison, 1978a) were ingested, required
intake would be 9.8-12.5 figs. These numbers of whole figs
correspond nicely to the 7 ? 2 nightly feeding passes observed
by Morrison (1978a) when A. jamaicensis was feeding
exclusively on fruits off. insipida.
In summary, A. jamaicensis has meager, if any, fat reserves;
probably exhibits extraordinary glucose assimilation, storage,
mobilization, and glycolytic capacities; probably has extreme
daily fluctuation in glycogen levels with little reserve capacity;
and is marginally able to maintain caloric balance on a normal
daily intake of 7 ? 2 Ficus insipida fruits. Ingestion of nine
fruits probably would allow A. jamaicensis to maintain a high
Tb for a 24-hour period but ingestion of fewer fruits would not
allow caloric balance as a high Tb homeotherm. Such bats
would conserve energy and thus remain in caloric balance by a
drop in regulated Tb, and a corresponding drop in energy needs.
Nitrogen Balance
Nitrogen excretion is related to metabolic rate. Conse-
quently, nitrogen requirements are appropriately related to
metabolic body mass (W?-75) (Brody, 1945; Kleiber, 1975). The
daily nitrogen requirement (mg/day) for high Tb homeotherms
is 200 W075, where W is in kilograms (National Research
Council, 1978). The nitrogen requirement can be converted to
a minimum protein requirement by multiplying by 6.25
(Herbst, 1988). Alternatively, dietary protein requirement can
be calculated as a function of ingested caloric intake. Minimum
protein for maintenance is 10.7 mg protein per Kcal ingested.
For a 45 g A. jamaicensis, the daily minimum protein
requirement is 122 mg, based on body mass alone. Using
maximal estimated daily energy expenditure (12.0 Kcal/day
from Table 2-1), calculated daily minimum maintenance
protein intake is 128 mg. The protein density of F. insipida fruit
juice is 4.7 mg/ml (calculated from Morrison, 1980b).
Assuming fig juice to be the only source of dietary nitrogen of
A. jamaicensis, constantly homeothermic individuals maintain-
ing high Tb would require 26.0-27.2 ml of fig juice/day (at
100% assimilation) to maintain nitrogen balance. This esti-
mated required intake is less than the calculated daily volume
of fig juice needed to maintain caloric balance in high Tb
homeothermic individuals (29.4?37.2 ml/day).
Digestibility of protein in low-fiber diets in a variety of
mammals ranges from 77% to 90% (Maynard and Loosli,
1969). Assuming an assimilation of 85% for A. jamaicensis,
daily minimum intake of fig juice would rise to 30.6-32.0
ml/day. This would mean that the daily volume of fig juice
necessary to meet protein needs is equal to or less than that
needed for caloric balance and that maintenance of nitrogen
balance is less of a problem for the bats than maintaining
caloric economy. The calculated protein minimum, however, is
for the "ideal" protein whose amino acid composition exactly
reflects the needs of the subject. Rasweiler (1977) pointed out
that animal proteins generally have amino acid compositions
that correspond more closely to mammalian requirements and
may be more readily digestible than proteins of plant origin,
which often are incomplete in terms of essential amino acids.
14 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
The calculated requirement for fig juice volume given above
is surely a minimum or low estimate of actual juice needs. As
is the case for caloric economy, it seems likely that a high Tb
homeotherm such as A. jamaicensis could maintain nitrogen
balance only marginally on a diet of F. insipida fruit. Again, the
ability of a free-living A. jamaicensis to reduce its regulated Tb
acts as a safety valve, not only for caloric balance, but also by
reducing dietary nitrogen requirements to a level sufficient to
allow nitrogen balance.
Although studies of the structure and function of kidneys of
Neotropical bats will be discussed in more detail with respect to
water and mineral balance, some of the data are pertinent to
nitrogen balance. Studier, Wisniewski et al. (1983) examined
kidneys in 25 species of Neotropical bats and suggested that
renal morphology is primarily a function of dietary protein
density. Among the phyllostomids, members of the primarily
frugivorous/nectarivorous subfamilies Glossophaginae, Carol-
liinae, and Stenodermatinae (including A. jamaicensis), most of
which have low-protein diets, possess renal medullae that
cannot be subdivided readily into inner and outer zones.
Members of the phyllostomid subfamilies Phyllostominae and
Desmodontinae, as well as all members thus far studied in all
other families of New World bats, have renal medullae that are
easily subdivided into inner and outer zones. The dietary
preferences of this second group of bats are varied, but all
species regularly consume some food of animal origin, which
is high in protein.
Our data on urine composition further support the proposed
relation between dietary protein density and renal function in
Neotropical bats (Studier and Wilson, 1983). We found urinary
ammonia and urea nitrogen levels for A. jamaicensis (495 mg%
N), although highly variable, to be markedly lower than levels
for the insectivorous species, Myotis nigricans (1887 mg% N).
If the minimal nitrogen requirement for a 45 g A. jamaicensis is
19.54 mg/day (= 200 x 0.045075), then total urinary N is 434
mg/kg/day, which approximates urinary nitrogen excretion
rates in many mammalian herbivores (Altman and Dittmer,
1961). If the two abnormally high values for urinary ammonia
and urea nitrogen we found in A. jamaicensis are disregarded,
the recalculated average level is 370 mg% N (n = 17, Studier
and Wilson, 1983).
Water Balance
We now have sufficient data to present a rough water balance
account for A. jamaicensis (Table 2-2). Values in Table 2-2
represent estimates for a 45 g, high Tb homeothermic
individual. As previously discussed, daily intake of fig juice is
29.4-37.2 ml. Swallowed juice is 90% water (Morrison,
1980b). Daily intake of water in food, therefore, is 27.6-34.9 g.
Estimated metabolic water assumes complete aerobic oxidation
of all glucose in the consumed juice (111 mg/ml, from Studier,
Boyd et al., 1983). The calculated value for metabolic water is
probably slightly low because oxidation of the small amounts
TABLE 2-2.?Water economy budget for a 45 g, high Tb, homeothermic
Artibeus jamaicensis. All values are g/day. EWL ? evaporative water loss. See
text for further details.
Parameters g/day
WATER GAINS
In food
From metabolism
Drunk
Total gain
WATER LOSSES
EWL at rest
EWL in flight
In urine
In feces
Total loss
UNACCOUNTED LOSSES
27.6-34.9
1.9-2.4
0
29.5-37.3
5.2
1.3
9.4-11.8
11.8-14.9
27.7-33.2
1.8-4.1
of dietary fats and proteins will produce a little additional
water. There is no indication that A. jamaicensis needs to
consume free water when feeding on figs. The studies of
Phillips et al. (1984) on gastric ultrastructure in Artibeus also
indicated a lack of importance of free water ingestion.
Assuming constant temperature and humidity, evaporative
water loss (EWL) at rest is calculated as
log EWL = log 0.398 + 0.672 log W
where EWL is grams of water/animal/day and W is in grams
(Studier, 1970). We estimated EWL in flight based on 45
minutes total flying time/day (Morrison, 1980b) and scaling up
the EWL (957 mg/h) found by Carpenter (1969) for flying
Leptonycteris sanbomi (24.4 g). Estimates of urinary water
loss and water lost in fecal matrix are derived from Morrison's
(1980b) data showing that urinary water represents 31.8% and
fecal water represents 40.1% of swallowed fig juice, respec-
tively. If all ingested nitrogen appeared in the urine, A.
jamaicensis would produce urine volumes of 4.0-5.3 ml/day,
assuming a minimum daily required nitrogen intake of 19.54
mg/day and urinary ammonia and urea nitrogen levels of
370-495 mg%. These values are considerably lower than
estimates based on Morrison's (1980b) data, but still represent
remarkably high urine output.
Considering the multiple sources and assumptions used to
construct the water economy budget for A. jamaicensis (Table
2-2), the values come remarkably close to balancing and are
probably accurate. Some useful comparisons can be made with
values for other mammals. Water turnover rates for a 45 g A.
jamaicensis (655-829 ml/kg/day) are extreme in contrast to
values of 40-273 ml/kg/day reported for a wide variety of
mammals (Altman and Dittmer, 1961). Similarly, preformed
water consumption in A. jamaicensis of 613-775 ml/kg/day is
elevated in comparison with values for other mammals
(35-211 ml/kg/day; Altman and Dittmer, 1961). These
NUMBER 511 15
exceptional values relate to the essentially liquid diet of A.
jamaicensis, coupled with its poor renal water conservation,
and relatively small size. Comparative values for total body
turnover and preformed water turnover are 330 ml/kg/day and
150 ml/kg/day, respectively, for an 8.4 g Myotis thysanodes
(O'Farrell et al., 1971), and 250 ml/kg/day and 180 ml/kg/day,
respectively, for M. lucifugus (O'Farrell et al., 1971). Total
body water turnover in Pizonyx (= Myotis) vivesi is estimated at
480 ml/kg/day (Carpenter, 1968). Preformed water turnover for
a common vampire, Desmodus rotundus, weighing 34.2 g is
410 ml/kg/day (Wimsatt, 1969), assuming bovine blood to be
78.5% water (McNab, 1973). Preformed water turnover also
can be estimated from published data for the nectarivorous bat,
Leptonycteris sanborni, at 465-712 ml/kg/day (Howell, 1974),
and the nectarivorous bird, Selasphorus flammula, at 692
ml/kg/day (Hainsworth and Wolf, 1972).
Urinary output in A. jamaicensis varies from 209 to 262
ml/kg/day in contrast to many other mammals with values that
vary from 2.5 to 74 ml/kg/day (Altman and Dittmer, 1961).
These rates of urine production in A. jamaicensis (6.5-8.2
microliters/min) are roughly 30 times the maximal rate of urine
production (0.23 microlitcrs/min) found by Bassett and
Wicbers (1979) for the insectivorous M. lucifugus. Having
collected urine samples from many species of bats, we have no
difficulty believing that rates of urine production in A.
jamaicensis and other frugivorous/nectarivorous bats far
exceed urine volumes considered normal in other species.
As mentioned earlier, A. jamaicensis and other frugivorous
and nectarivorous bats possess kidneys with undivided renal
medullae. Such species routinely produce natural urine of low
osmotic pressure and low urinary nitrogen levels (Studier and
Wilson, 1983) compared with those species with renal medulla
divisible into inner and outer zones (Studier, Wisniewski et al.,
1983). Mean maximal urine concentration (MMUQ in A.
jamaicensis is 972 mOsm/kg (Studier, Boyd et al., 1983). The
total medullary (M) thickness to cortical (C) thickness ratio
(M/C) for A. jamaicensis (2.4), while typical for frugivores, is
markedly lower than M/C for bats of other feeding preferences
and does not vary with habitat aridity (Studier, Wisniewski et
al., 1983).
Geluso (1980) presented a highly predictive equation
relating MMUC of insectivorous bats to M/C in which MMUC
(mOsm/kg) = 702 + 387 (M/C). Based on this equation, A.
jamaicensis would produce MMUC of 1,620 mOsm/kg, a value
nearly double the observed MMUC. Similar observations hold
true for other frugivorous/nectarivorous species with undivided
renal medullae (Carpenter, 1969; Studier and Wilson, 1983).
None of these species produce natural urine concentrations
approaching those predicted by Geluso's equation, suggesting
that his formula does not apply to bats with undivided renal
medullae (Studier and Wilson, 1983).
We made several attempts to induce MMUC in A.
jamaicensis, that included dehydration/starvation, loading with
strongly hyperosmotic salt solutions, and feeding dehydrated
fruits of figs (Studier, Boyd et al., 1983). Although none of
these methods worked well, ingestion of dehydrated figs, the
functional equivalent of Geluso's (1975, 1978) "water denied"
experiments with insectivorous bats, resulted in the most
uniform and highest urine concentrations for this species. It is
of particular interest that although dehydration and salt loading
caused an expected and predictable increase in osmotic
pressure of the blood, these treatments were not associated with
the expected increase in osmotic pressure of the urine (Studier,
Boyd et al., 1983). Dehydration in Myotis lucifugus, induced by
Bassett and Wiebers (1979), however, resulted in expected
increases of osmotic pressures in both blood and urine. There
seems to be a slow or minimal release of antidiuretic hormone
(ADH) or a slow or reduced renal tubular response to ADH in
response to rising osmotic pressure in the blood of A.
jamaicensis.
Urine samples taken from A. jamaicensis at sunset in May
were significantly more concentrated and less variable than
samples taken in November (Studier, Boyd et al., 1983). The
May samples were taken at the end of the dry season and the
November sampling occurred toward the end of the wet season
(Smythe, 1974). Presumably heat/dehydration stress is greater
in the dry season than in the wet. In May, there was a marked
rapid decrease in total urine concentration 0.5-1.5 hours after
sunset in free-flying A. jamaicensis. This decrease is associated
with rapid food passage time in this species, ingestion of
adequate hypotonic fluid for rehydration, and rapid assimila-
tion and equilibration with the ingested fig pulp juice. Urine
then became progressively more concentrated throughout the
remainder of the night. Osmotic pressures of urine in captive,
rehydrated (taken two hours after sunset) individuals were
identical throughout the night with urine concentrations of
free-flying A. jamaicensis (Studier, Boyd et al., 1983). This
suggests that rehydration occurs early in the nightly feeding
period and is unaffected by subsequent feeding bouts. We
know from other studies that A. jamaicensis feeds sporadically
throughout the night (Morrison 1978a; 1978b; 1978c).
Mineral Balance
How herbivorous mammals ingest adequate amounts of
dietary sodium (Na+) has generated considerable interest
(Blair-West et al., 1968; Cowan and Brink, 1949; Dalke et al.,
1965; Herbert and Cowan, 1970; Jordan et al., 1973; Stockstad
et al., 1953; Weeks and Kirkpatrick, 1976; 1978). Sodium
levels in most plants and plant parts are typically low (Likens
and Bormann, 1970; Sauchelli, 1969; Weeks, 1978) and related
to soil Na+ levels, which in turn are highly affected by the Na+
levels in rainfall (Blair-West et al., 1968) and the frequency of
rainfall. Tropical rain forest may be particularly susceptible to
loss of nutrients by leaching due to rapid decomposition of
litter and heavy, frequent rains (Jordan and Herrera, 1981).
Although some data on characteristics and composition of the
soils of BCI are available (Knight, 1975), there is no
16 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
information on soil sodium levels.
Fig fruits contain little sodium (Diem, 1962; Heinz Interna-
tional Research Center, 1964; Oates, 1978). Sodium levels in
ripe fruits of F. insipida and F. yoponensis have been measured
at 0.49 and 0.48 mg/g dry weight, respectively (Nagy and
Milton, 1979). We determined sodium levels in figs carried by
A. jamaicensis to be similar to those found by Nagy and Milton
(1979), but potassium concentrations were lower (Studier,
Boyd et al., 1983). Sodium density in dried pulp is about 2.4
times the sodium level of dried seeds and is identical to the
sodium level of pulp juices. Thus, the consumption of fig juice
rather than the entire fruit greatly increases dietary Na+ density
in A. jamaicensis and significantly reduces the weight of figs
estimated to be required for maintenance of Na+ balance. On
the other hand, the K+ level of fig juice is less than half the
concentration of that ion in dried pulp. This implies that K+ is
concentrated in specific organelles within the fig pulp and is
not likely to be extracted by A. jamaicensis. It is released in the
process of homogenization of the dried pulp for laboratory
analysis. The lowered dietary K+ level obtained from pulp
juices as opposed to whole pulp probably also lowers the Na+
requirements of A. jamaicensis as it does in other mammals
(Meyer et al., 1950; Staaland et al., 1980; Weeks and
Kirkpatrick, 1978).
Minimal sodium requirements have been estimated for few
small mammals. Sodium required for growth in laboratory rats
and mice is estimated at 10 and 18 mg/animal/day, respectively
(National Research Council, 1978). Assuming the average
requirement for growth in A jamaicensis is 14 mg/animal/day,
bats would require 69 ml (72 gms) of F. insipida fruit juice at
8.8 mEq/L sodium level to maintain sodium balance. Such
amounts far exceeds the requirements of fig juice previously
calculated for maintenance of caloric and nitrogen balance
(29.4-37.2 and 30.6-32.0 ml/day, respectively). Estimated
daily Na+ requirements for growth are probably higher than
requirements for maintenance. However, it would appear that
acquiring adequate sodium for daily requirements from fig
juice is more likely to be a nutritional limiting factor than
ingestion of sufficient juice to meet caloric and nitrogen needs.
Mammals suffering Na+ deficiency characteristically exhibit
hypertrophy and hyperplasia of the zona glomerulosa of
adrenal glands and greater development of striated and
excretory ducts within salivary glands (Blair-West et al., 1968).
These features, acting through the renin-angiotensin-
aldostcrone system, result in renal and salivary Na+ retention.
The adrenal zona glomerulosa of A. jamaicensis shows no
obvious hypertrophy or hyperplasia when compared with the
condition in Neotropical insectivorous bats, although possible
subtle differences may yet be detected (Studier, Boyd et al.,
1983). We have not found an increase in the number of ducts
within salivary glands, another fact that argues against a
probable Na+ deficiency in A. jamaicensis. The inordinate size
of these glands, however, indicates a proportionate increase in
absolute number of ducts per gram of body mass of the bat.
Energy and Water Balance during Lactation
Because the foregoing discussion has concerned nutritional
requirements and balances needed for maintenance, it is useful
to estimate nutritional increments needed under stress such as
during lactation (see Section 3, Reproduction in a Captive
Colony). A 45 g A. jamaicensis should produce milk at a rate of
12.3 gm/day based on Linzel's (1972) measure of milk
production as a function of body mass (daily milk production in
Kg/day = 0.126075 Kg/Kg). Milk of A. jamaicensis contains 2.3
Kcal/g (Jenness and Studier, 1976). This energy level is
comparable to milk energy content for other bats, but is higher
than milk energy levels for many large mammals. The high
energy content of A. jamaicensis milk is in accord with Ben
Shaul's (1962) suggestion that mammals that nurse their young
on a scheduled basis produce milk of higher energy content
than mammals that nurse continuously or on demand.
If one assumes that food energy can be converted to milk
energy with no cost, the production of 12.3 g of milk per day at
2.3 Kcal/g imposes a minimal additional caloric requirement
for A. jamaicensis of 28.3 Kcal/day. This would raise the total
daily caloric requirement to about 40 Kcal/day for a high Tb,
homeothermic, lactating female compared to 12.0 Kcal/day for
a nonlactating individual. The total milk protein level for A.
jamaicensis is 4.7 g% (1.1 g% casein and 3.6 g% whey protein)
(Jenness and Studier, 1976). Again assuming no energy costs
for milk protein synthesis, a high Tb, homeothermic, lactating
female would require an additional incremental daily protein
intake of 578 mg for a total daily protein requirement of
700-706 mg compared to 122-128 mg/day for a nonlactating
individual. Milk of A. jamaicensis is about 70% water;
therefore, production of 12.3 g of milk would require an
additional intake of 8.6 ml of water for a total daily water need
of 38.1-45.9 ml in lactating females compared to the
29.5-37.3 ml water requirements for nonlactating bats.
During lactation, therefore, the additional incremental needs
for extra caloric and nitrogen intake are massive in comparison
to additional water needs. Whereas estimated milk production
may seem somewhat high, energy efficiency for milk produc-
tion is certainly not 100%. Brody (1945) calculated gross
energetic efficiency of milk production to be 28%-34% for
humans and 44%-48% for rats. We suggest that during periods
of high nutritional demands, such as growth and especially
pregnancy and lactation, A. jamaicensis would be expected to
lower their regulated Tb to reduce caloric and nitrogen needs
and that during such times, these bats may supplement their
staple fig diet with food items of higher caloric and protein
density. Studies directed at shifts in food habits during
pregnancy and lactation could test this hypothesis.
Summary
Studies on energy balance in A. jamaicensis were focused on
this bat's use of the fruits of Ficus insipida, the food that it used
NUMBER 511 17
most on BCI. Probably these bats always are in slight food
stress in the wild and are more likely to behave as facultative
heterotherms. Poor body temperature regulation in newly
captured bats is not related to physiological competence, but
reflects reduced metabolic heat production and rate of depletion
of energy stores. A. jamaicensis falls very near the minimum
boundary curve for high body temperature homeothermy,
suggesting that energy savings from heterothermy may be
critical to this bat in the wild.
Artibeus jamaicensis has extremely low fat reserves and a
high intake of dietary carbohydrate, suggesting that glycogen
may be its normal energy reserve. This bat, in its natural
environment, maintains no significant positive daily energy
balance that would allow for storage of surplus caloric energy.
The energy cost of basal metabolism represents the major
fraction (55%-83%) of total daily energy requirements. Daily
energy budgets of 10-12 Kcal/day combined with the caloric
content of daily food intake requires an intake of 9.8-12.5 figs
per day, a figure not inconsistent with the 7 ? 2 nightly feeding
passes observed in radiotelemetry studies.
Nitrogen and protein requirements can be met by the amount
of daily food intake necessary to maintain caloric balance,
although questions remain about the digestibility of plant
proteins. Urinary ammonia and urea nitrogen levels are
markedly lower in A. jamaicensis than in bats that use animal
protein.
Based on our studies of caloric, nitrogen, and water balances,
there is no indication that A. jamaicensis needs to consume free
water when feeding on figs. Water turnover rates for A.
jamaicensis (655-829 ml/kg/day) are extreme in contrast to
values reported for a wide variety of other mammals. Mean
maximal urine concentration in A. jamaicensis is 972 mOsm/
kg, a strikingly low value indicating poor urine concentrating
ability. Published predictive equations for maximal urine
concentration do not apply to frugivorous bats. Dehydration in
A. jamaicensis results in increased blood osmotic pressure, but
without a concomitant increase in urine osmotic pressure.
Sodium is potentially limiting in tropical animals restricted
to a frugivorous diet, but structural features of the kidneys and
salivary glands of A. jamaicensis argue against any probable
chronic sodium deficiency in these animals. During periods of
high nutritional demands such as growth, pregnancy, and
lactation, A. jamaicensis probably lowers its regulated body
temperature to reduce caloric and nitrogen needs and may use
other, more energy- and protein-rich food resources.

3. Reproduction in a Captive Colony
Lucinda Keast Taft and Charles O. Handley, Jr.
We report on the reproductive biology of Artibeus jamaicen-
sis based upon studies of a colony held captive at the National
Zoological Park (NZP). Although information is available on
many aspects of the reproduction of bats, most is based on
temperate zone Vespertilionidae. The most recent reviews of
pre- and postnatal development among the vespertilionids are
those of Orr (1970) and Tuttle and Stevenson (1982). Racey
(1988) summarized methodology for reproductive assessment
and Wilson (1988) provided information on maintaining bats
for captive studies. There is little information, however, on
reproduction and ontogeny of other bats. Kleiman and Davis
(1979) reviewed the available literature on development and
maternal care in phyllostomids. The most detailed information
on ontogeny is for Carollia perspidllata (Kleiman and Davis,
1979) and Desmodus rotundus (Schmidt and Manske, 1973).
Phyllostomid bats show far greater diversity of social
systems, dietary habits, reproductive strategies, and selection of
roost sites than do the vespertilionids (Baker et al., 1976,1977,
1979). The selective pressures with which phyllostomids must
cope are quite different from those encountered by the
better-known vespertilionids of the temperate zone. Compari-
sons between the two families should be productive.
Each year most female A. jamaicensis give birth to a single
young during two reproductive episodes. This pattern of
bimodal polyestry is common to many Neotropical frugivorous
and nectarivorous bats (Wilson, 1979). A. jamaicensis is
unusual, however, because development of the implanted
blastocyst is delayed for 2.5-3 months during one of the birth
episodes (Fleming, 1971; Fleming et al., 1972). Delayed
development has been documented only in Panamanian
populations of A. jamaicensis, but it is likely to prove
widespread. Delayed development also occurs in a phylo-
genetically and ecologically diverse array of bats, Macrotus
(Bradshaw, 1962), Miniopterus (Medway, 1971), Hipposideros
(Bernard and Meester, 1982), and Haplonycteris (Heideman,
1988).
Lucinda Keast Taft, National Zoological Park, Smithsonian Institu-
tion, Washington, D.C. 20560.
Charles O. Handley, Jr., National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560.
Parturition and neonatal appearance have been described
(Bhatnagar, 1978; Jones, 1945,1946), but little is known about
early development of the young. In Panama^ where the young
of A. jamaicensis usually are bom in tree holes (Morrison,
1975), the study of early development is difficult because many
tree hole roosts are inaccessible and the bats show a strong
tendency to desert a roost if disturbed. Therefore, observations
on captives is still the best means of gaining information on
reproduction and development.
Novick (1960), who was successful in breeding and
long-term maintenance of A. jamaicensis in captivity, believed
that freedom from handling was necessary for successful
reproduction. Improved artificial diets (Rasweiler and de
Bonilla, 1972) have enhanced the successful maintenance of a
number of Neotropical frugivorous and nectarivorous phyllos-
tomids (Greenhall, 1976; Rasweiler, 1975,1977; Rasweiler and
de Bonilla, 1972; Rasweiler and Ishiyama, 1973). Kleiman and
Davis (1979) found that captive Carollia perspidllata success-
fully bred in spite of the handling necessary for weekly
examinations of the adults and young.
History of the Research Colony at NZP
We established a research colony of A. jamaicensis at the
NZP in Washington, D.C, with 24 bats captured in June 1978
near Corozal, Panama^ 35 km SE of Barro Colorado Island
(BCI). We studied reproduction and development in this colony
from July 1978 through August 1981 and, consequently, we
can describe several aspects of the biology of A. jamaicensis in
considerable detail.
Among the original 24 bats, three males and 12 females were
subadults, born early in 1978. Four males and five females were
adults. The females were neither lactating nor obviously
pregnant at capture. Prior to the first births in captivity (January
1979), two adult males and four subadult females died. One of
these was a female that apparently did not adjust to the captive
feeding regime. On the 47th day of captivity all bats were
wing-banded with plastic bands and three days later another
female died, possibly of complications from banding-
associated trauma. The other four bats died because of
19
20 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
unspecified pathological conditions. Subsequently, no addi-
tional deaths occurred among the original animals during the
next 2.5 years.
Three captive-born males (one adult and two subadult) were
removed to another cage on 18 February 1980 to reduce
crowding and aggression in the flight cage. On 10 October
1980 and 24 June 1981, ten and 12 bats, respectively (including
two original females that had repeated reproductive failures),
were removed for the same reasons.
Routine handling did not appear to harm the bats in our
colony as conception rates were extremely high, particularly for
parous females. Exceptions were cases where young were
handled frequently during the first three days postpartum. The
accompanying disturbance to the mothers sometimes caused
maternal abandonment and death of the young. Bats that died
before the end of the study were necropsied by the NZP
Department of Pathology to determine cause of death.
At the NZP, we kept our bats in two adjoining, climate-
controlled rooms, each measuring 3 x 3 x 2.5 m with free
access between them through a 1 x 2 m door. The temperature
was maintained at approximately 29?C (25?-31?C) and the
relative humidity kept above 50% (range, 50%-80%). After
one month of habituation, the bats were clock-shifted a half
hour every other day until they were on a reversed light cycle
(light, 2000-0800 hours).
Each room contained a burlap-lined wire mesh box, 0.5 x 0.5
x 1 m, open at the bottom, about 1.5 m above the floor. These
were intended to be roosts, but the bats preferred the open wire
mesh-covered ceilings. Food and water cups were hung on wire
brackets on one of the roost boxes, and tree branches were laid
across the top of the box. At the beginning of each dark cycle,
the bats were provided with a supplemented, peach nectar-
based diet (Rasweiler and de Bonilla, 1972) and water ad
libitum. Partially opened, ripe bananas were suspended from
the branches by rubber-coated wire.
Adult bats were marked with one or two plastic bird bands
(A.C. Hughes, 1 High Street, Hampton Hill, Middlesex, TW12
1NA, England) applied to the left forearm of males, and the
right of females. Each bat received a unique color combination
so that individuals could be recognized without capture. Bands
were not applied to young bats until skeletal growth was
complete (about 12 weeks of age). Soon after birth the young
were punch-marked with a number on the wing membrane
using a tattooing device (Bonaccorso and Smythe, 1972). It was
usually necessary to repeat the tattooing process two or three
times before the bats were old enough to be banded because the
punch-mark holes healed and faded rapidly (Kleiman and
Davis, 1974).
For periodic physical examinations, one of the two adjoining
flight rooms was closed off with a burlap curtain and kept
darkened. Bats were captured in butterfly nets in the lighted
room and released into the dark room after examination. We
conducted bimonthly examinations of the adults. The young
were examined every two or three days until they were nine
weeks old, weekly until 12 weeks old, and then bimonthly
thereafter. After pregnant females were found, the colony was
carefully inspected each day for births.
In each capture session, the bats were placed in snug-fitting
paper tubes and weighed to the nearest 0.1 g. Several external
characteristics that vary with reproductive condition were
examined and described. These included vulval coloration,
mammary size and appearance, and testis size. Lactation was
confirmed by gently massaging the areola until milk was
expressed from the nipple. Palpation of the abdomen revealed
pregnancy.
From the records of these regular examinations we devel-
oped criteria for categorizing nipple size and condition, and
testis size that we used at the NZP and on BCI to describe age
and reproductive state. At the NZP we were able to assign real
time to the age categories that we used in the field on BCI (see
Appendix). In our study at the NZP we added two categories to
distinguish younger juveniles: (A) neonate (day one), babies
during the first 24 hours after birth; and (B) infant (two to about
30 days of age), a category to distinguish nonvolant young
from juveniles capable of independent flight.
The forearm was measured with dial calipers to the nearest
0.1 mm and wing span was measured with a metric ruler to the
nearest 5.0 mm. Wing area was determined by outlining the
completely outstretched right wing on paper. A straight line
was drawn from the point where the leading edge of the wing
joined the body to the point where the trailing edge joined the
foot (Davis, 1969a). Area to the nearest 0.1 cm2 was then
determined with a Hewlett-Packard 9874A digitizer and
doubled to account for the area of both wings.
General physical condition, genital appearance, degree of
epiphyseal fusion, pelage growth, and dental development were
monitored at each examination of the young bats. The ability of
neonates to emit ultrasonic vocalizations was determined with
a QMC Mini bat detector (QMC Instruments, Ltd., 229 Mile
End Road, London E14A A, England).
Flight development was determined by tests in which the
young were dropped from a height of six feet into a net and
scored according to the following criteria:
Drop: fell into the net without spreading the wings.
Spread: wings were extended, but not flapped, while the bat
fell straight down.
Flap: wings were flapped while the bat fell straight down.
Glide: some forward motion was achieved with flapping, but
no altitude was gained.
Gain: altitude was gained, but landing and maneuvering
skills were not exhibited.
Hang up: showed ability to maneuver around obstacles and
land by flipping the feet over the head to hang inverted in the
roost.
We observed individual behavior through windows in the
walls of the flight rooms. Rheostat-controlled, low-level
incandescent lighting facilitated observations after short peri-
NUMBER 511 21
ods of habituation. Prior to the birth of young, the colony was
watched for a minimum of six hours per week. Offspring of the
first birth group (BG-I), early spring 1979, were each observed
for at least three hours per week, with the result that the general
behavior of all the colony individuals was incidentally
monitored for six to 30 hours per week from 29 January to 25
July 1979. We used the focal animal technique for observations
on infants and juveniles and recorded on a checksheet. Here we
only report the behavioral patterns, such as flight, that are
dependent on the physical development of the young.
Statistical analyses followed techniques recommended by
Sokol and Rohlf (1969). We used appropriate parametric tests
when required assumptions were met; otherwise nonparametric
tests were used. Mean and standard deviation or variance were
used as standard measures of central tendency and variation.
Some statistical analyses and the plots of growth of several
measured characters were made with the Statistical Analysis
System (Helwig and Council, 1979) at the George Mason
University Computer Center, Fairfax, Virginia.
Characteristics of Adults
SIZE.?Measurements of the original wild-caught individu-
als were taken after 125 and 305 days of captivity when all
definitely had reached the adult age-class. Females were larger
(but not significantly) than males in mass and forearm length.
Other measures of wing size (span, area, width, and length of
tip) were significantly larger in females (Table 3-1).
We found less difference in forearm lengths of adult males
(X = 62.1 mm, range 57-68, n = 30) and females (X = 62.3,
range 59-68, n = 30) on BCI than in the NZP colony (X = 61.3,
n = 7 in males; X = 62.4, n = 12 in females). The average mass
of adult males from BCI was consistently less than 50 g (48.5
g, n = 100), while averages of nonpregnant females were
greater than 50 g (51.1 g, n = 100). Mean mass of the NZP bats
was 51.1 g in males and 54.3 g in females. Female-to-male size
ratios among the captives show that females were from two to
nine percent larger than males in various wing measurements
and about six percent heavier in mass (Table 3-1).
Forearm and mass measurements indicating that females are
larger than males in this species have been published (Goodwin
and Greenhall, 1961; McManus and Nellis, 1972; Rails, 1976;
Silva Taboada, 1979), but the magnitude and significance of
the differences were not mentioned in those reports. Wing-
loading values (body mass in g/wing area in cm2) were
significantly greater in males over similar-sized females in A.
jamaicensis from the Virgin Islands (McManus and Nellis,
1972).
Female vespertilionids generally are larger than males in
mass and forearm length, but significant differences in skull
measurements are not evident (Myers, 1978; Williams and
Findley, 1979). Species where females must carry relatively
greater litter weights were predicted to show greater degrees of
dimorphism with respect to wing size (Myers, 1978).
Although their data did not support the Myers' (1978)
hypothesis, Williams and Findley (1979) agreed that the need
for greater weight bearing capacity should select for larger size
in female bats. Comparable studies of sexual dimorphism have
not been reported for the phyllostomids.
APPEARANCE OF NIPPLES.?1. Preparturient Condition: The
eight wild-caught females recognized as subadults in the
summer of 1978 produced offspring in Birth Group I (BG-I) in
the spring of 1979. Their tiny (- 0.5 mm diameter), unpigmen-
ted, hairy nipples (hairy and naked in this discussion refer to the
condition of the areola) began to show enlargement (to 1.0-2.0
mm diameter) almost four weeks before we were able to detect
fetuses (X = 3.75 weeks prior to fetal detection; SD = 3.105;
range, 0.0-8.0 weeks before fetal detection; all statistics ? one
week). Over the following two weeks the nipples grew in size
and shed hair until attaining the large (-6 mm diameter) and
naked condition at an average of 1.5 weeks prepartum (range,
0.5-3.0 weeks prepartum; SD = 0.926; all statistics ? one
week). Once the large size was reached, the nipple skin
appeared pigmented (darkened) in all but one of the females.
The correlation between the first detectable change in size of
nipples and first pregnancy in subadult females has not been
TABLE 3-1.?Measurements of wild-caught adult Artibeus jamaicensis from central Panama.
Variable
Mass (g)
Forearm (mm)
Wing span (mm)
Wing area (cm2)
Wing width (mm)
Wing tip (mm)
Female, N
mean
54.3t
62.4
472.5
281.6
93.1
117.5
= 12
SD
3.888
1.859
12.154
25.518
4.641
4.101
Male, A
mean
51.1
61.3
448.6
258.8
85.6
107.7
r = 7
SD
4.771
1.746
8.997
19.381
6.024
8.077
' .
1.594
1.271
4.512
2.038
3.051
3.540$
Student's f-test
P*
ns
ns
<0.0005
<0.05
<0.005
<0.005
Female/Male
1.063
1.018
1.053
1.088
1.088
1.091
* One-tailed.
t An average non-pregnant fasting mass was determined for each female and then these were averaged.
t The variances of wing tip measures were not homoscedastic; therefore a Wilcoxan two-sample test was also performed (U, = 75.5, P <0.005).
22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
noted for other species of bats, although Kleiman and Davis
(1979) reported darkened nipples in parturient Carollia
perspicillata.
2. Postlactating Condition: We examined regression of
nipples after lactation to a smaller size following each of the 51
births involving the original 13 females. In 14 out of 38 cases
where weaning was completed, nipples regressed to a small
size (-1.0-2.0 mm diameter) after an average of 124.3 days
(80-188 days; SD = 32.511). However, they did not regress
below medium size (-4.0 mm diameter) in the other 24 cases
(63%). Out of 13 instances in which infants died before
weaning, there was one example of nipples not shrinking below
medium size and 12 where the nipples reached small size by an
average of 20.2 days (5-36 days; SD = 8.167) after death of the
infant. Nipples of postlactating females did not regress to the
tiny size (0.5 mm diameter) characteristic of subadults.
In all cases where nipples regressed to the small size, there
were other characteristics indicative of adult age (e.g.,
pigmentation of the nipple skin, and/or wholly or partially
denuded condition of the areolar region). Apparently, the
pigmentation of the nipples does not completely disappear after
lactation. Regrowth of fur around the nipple was slow, and
evidently it did not surround the nipple as closely as in
nulliparous females. The fur surrounding the nipple was
noticeably sparser than the rest of the ventral fur, even after
regrowth was completed, but the new hair was conspicuous
because it was darker than the surrounding old hair. It was a
sure indication of a postlactating condition.
3. Comment: The appearance of the nipples has been used in
bats to assign females to various age classes (e.g., Dwyer, 1963;
Pearson et al., 1952). Enlarged, darkened, and denuded nipples
typically indicate previous birth experience and thus adulthood.
In addition, size and color of nipples and condition of areolar
hair, together with vulvar coloration and other reproductive
indicators such as an embryo or milk can pinpoint any stage in
the reproductive cycle. Our observations indicated that these
criteria were valid for aging and determining reproductive
status in female A. jamaicensis, so they were used in the NZP
colony and in the mark-recapture studies on BCI.
TESTES ? Fleming et al. (1972) showed that periods of
testicular enlargement correspond to periods of female estrus in
Panamanian and Costa Rican populations of A. jamaicensis,
Uroderma bilobatum, and Carollia perspicillata. When our
original seven males arrived at the NZP the length of the testes
was 5 mm or less (X = 4.3) in the three subadults, and ranged
from 6-11 mm (X = 8.0) in the four adults. Because the colony
was established in July, which would have been during a period
of sexual receptivity for postparturient females, the adult males
should have exhibited maximum testicular length. This
apparently was the case, for a decline in length was apparent
after one month in captivity. This decline continued for 2.5
months until mid-October 1978, when the size of the testes in
adults averaged 6.3 mm. During the same period, the size of the
testes in the three subadults increased to an average of 6.0 mm.
Thereafter, testicular size increased in all the males, reaching
maximum size (X = 8.2 mm; n = 5) in early February 1979 near
the beginning of BG-I. A slight reduction in size (to 7.6 mm)
occurred at the end of BG-I, but size increased again at the
onset of BG-II. Size of the testes did not regress much after
BG-II. Through the following years of observation, testes of
most adult males remained above 7.0 mm and some remained
as high as 10.0-11.0 mm.
During the colony's first two and a half years, the observed
maximum testicular length was 11.0 mm; but later, testes up to
14.0 mm long were noted occasionally. Maximum hypertrophy
continued to coincide with birth peaks, but minimum length of
testes never fell below 9.0 mm during the remainder of the
study.
Reproductive Cycle
ESTRUS AND COPULATION.?Copulatory behavior was first
seen in August 1978, but births did not occur until January
1979. As a six-month gestation period is unlikely, delayed
development of the implanted blastocyst (Fleming, 1971)
probably occurred in females that had conceived. However,
some copulations were noted as late as November. Subse-
quently, we often saw copulations by newly parturient females,
indicating postpartum estrus. Newborn infants were usually
attached to the mothers during the copulations.
Males showed increased interest in the females even before
parturition, but successful copulation did not occur until day 2
postpartum. The greatest frequency of copulations or attempts
to copulate occurred on days 3 and 4 postpartum. This activity
was observed only sporadically thereafter. The latest copula-
tions (two) occurred 25 days postpartum.
A darkening of the vaginal rim of the vulva was noted on the
day of parturition. During the subsequent week, the darkened
area became more extensive, extending laterally as much as 4
mm, and becoming nearly black in color. During this period,
the males frequently attempted to copulate. Up to four
copulations or attempted copulations per female per hour were
recorded. Over the following 4-18 weeks the darkened vulval
area regained normal coloration. The vulval rim was the last
area to fade.
PRENATAL CHANGES.?The minimum observed interbirth
interval was 112 days. This figure compares well with the
four-month gestation that Fleming (1971) postulated for
Panamanian A. jamaicensis. We could detect the presence of a
fetus by palpation about six weeks before birth (X = 40.8 days,
SD = 6.19, n = 12). Earlier than this, there was the possibility of
mistaking the left kidney for a small embryo, although feeling
both the kidney and the embryo should have been a positive
clue. Later, when the female's abdomen was noticeably
distended by pregnancy, the head, legs, and feet of the
transversely positioned fetus could be felt. The maximum
NUMBER 511
90n
23
80-
~ 70H
O)
60H
50-
40 J
-90 "80 "70 -60 "50 "40 "30
DAYS PREPARTUM
-20 "10 O
FIGURE 3-1.?Body-mass changes in pregnant Art ibeus jamaicensis in the NZP colony. Daily means, standard
errors, and ranges are shown.
transverse abdominal extension in pregnant females was -50
mm (= crown-rump length of embryo).
When disturbed, pregnant females were more reluctant to fly
than other bats, and they flew more slowly and had difficulty
maneuvering. They frequently collided with obstacles or
dropped to the floor and were much easier to capture with a
hand net. When left alone, they returned to roosting areas.
Morrison (1980c) has observed reduced flight speed in
free-ranging A. jamaicensis carrying young.
Mass of females on the day before birth ranged from 68 to 81
g (X = 73.3 g), almost 35% more than normal nonpregnant
mass (Figure 3-1). Weight changes of pregnant females have
been reported (Kleiman and Davis, 1979) for only one other
phyllostomid, Carollia perspicillata. Female C. perspicillata
gained an equivalent of about one third of their nongravid mass
24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
during pregnancy. Their gestation length was probably 115 to
120 days. This is similar to the data we recorded for A.
jamaicensis. Both species exhibit transverse fetal positions
prior to birth. C. perspidllata also has a postpartum estrus
(Kleiman and Davis, 1979).
PARTURITION.?We did not observe any births. Apparently
they occurred during the light cycle (2000-0800 hours) or late
in the dark cycle (1800-2000 hours, actual time) when we were
not watching. From one to 14 hours may have elapsed between
actual birth and our initial examination.
No behavioral cues were detected in females about to give
birth. Adult females tended to form one large, tight group just
before the light period. In the later stages of pregnancy, they
frequently participated in the formation of temporary tight
groups even during the dark period.
Jones (1946) watched a birth in a captive "Artibeus
planirostris trinitatis" (= A. jamaicensis) from Trinidad. The
female hung head-down, and presented the young head first.
The baby hung by itself when only a few hours old.
LACTATION.?Milk was expressible from a mother's nipples
on the day of birth. Average duration of lactation for all
mothers of infants surviving past weaning age was 66.3 ? 7
days (n = 37; SD = 12.758; range, 46-95 days). Because
females were examined only bimonthly for expressible milk,
these figures were obtained by averaging the midpoints
between the last day females were observed lactating and the
first day they were noted to be dry.
Duration of lactation was analyzed by birth group, but single
classification analysis of variance (ANOVA) did not reveal
significant differences in duration of lactation between groups.
However, mean duration of lactation for BG-II and BG-IV were
both greater than the means for the other groups (Table 3-2).
BG-I, BG-III, and BG-V were intervals when lactating females
probably were simultaneously carrying embryos undergoing
TABLE 3-3.?Duration of lactation in females of the NZP colony of Artibeus
jamaicensis in episodes of normal and delayed gestation. /f = 1.896, one-tailed
Student's t-lest,P < 0.05.
TABLE 3-2.?Duration of lactation by
Artibeus jamaicensis.
Birth
I
II
III
IV
V
Mean duration
of lactation
in days
65.6
76.6
66.7
68.5
60.0
(range)
(47-77)
(57-94)
(52-87)
(54-95)
(50-87)
birth group
Number of
females
8
5
7
7
10
in the NZP
X2
35120.00
30078.50
32255.50
34004.25
37227.50
colony of
SD
9.761
13.608
13.540
13.895
11.679
Model II ANOVA
Source
Among
Within
Total
SS
966.023
4893.754
5859.777
4f
4
32
36
MS
241.506
152.930
F
1.579
P
ns
Development
Normal embryonic devel-
opment in females lactat-
ing during BG-I, III, and
V.
Delayed embryonic devel-
opment in females lactat-
ing during BG-II and IV.
Mean duration
of lactation
in days (range)
63.7 (47-87)
71.9 (54-95)
Number of
females
25
12
SD
11.591
13.786
normal intrauterine growth, whereas arrested embryonic devel-
opment characterized females gestating during BG-II and
BG-IV.
When the data of BG-II and BG-IV were compared with
those of BG-I, BG-III, and BG-V the two sets were
significantly different at the 0.05 level (Table 3-3). Lactation in
females carrying embryos during delayed embryonic develop-
ment persisted approximately eight days longer than lactation
during normal embryonic development.
Reproductive Rates
Information on six birth groups (BG-I to BG-VI) is given in
Table 3-4. Only one wild-caught female (F14) failed to produce
an infant during BG-I, but she gave birth nearly eight weeks
past the last birthdate of other bats of that birth group. Two
weeks later, an aborted fetus (about one-half normal neonate
size) was found on the floor. One month later, the other
pregnant females began having their second babies. Thus the
length of BG-II was increased by almost six weeks in order to
include these two birth events.
Wild-caught and captive-born females with prior birth
experience (multiparous) had high conception rates, 91.7% and
85.7%, respectively (Table 3-5). However, conception rates
were lower for captive-born females (-70%) during the first
birth group following their transition to adulthood, as shown by
the expected values obtained in an r-by-c contingency table
(Choi, 1978). Some pregnancies may have gone undetected
because of abortion or early fetal resorption.
Each female gave birth to only one offspring. Primary sex
ratios did not differ significantly from unity for individual birth
groups, or overall, or for infants born to wild-caught versus
those born to captive-born females (Table 3-6). Most phyllosto-
mids produce a litter size of one (Humphrey and Bonaccorso,
1979), although twin embryos have been found in low
frequency in a few species, including A. jamaicensis (Barlow
and Tamsitt, 1968). A female vampire produced twins in
captivity, one of which was apparently stillborn (Burns, 1970).
NUMBER 511 25
TABLE 3-4.?Summary of reproduction and mortality in the NZP colony of Artibeus jama ic ens is.
Birth
group
I
II
III
rv
V
VI
Total
Dates
of birth
01.29.79 to 03.07.79
05.01.79 to 08.01.79
11.28.79 to 01.31.80
04.21.80 to 06.16.80
11.05.80 to 12.21.80
03.04.81 to 04.30.81
Origin of
females
Wild-caught
Wild-caught
Wild-caught
Captive-bom (primiparous)
Wild-caught
Captive-born (multiparous)
Captive-bom (primiparous)
Wild-caught
Captive-bom (multiparous)
Captive-born (primiparous)
Wild-caught
Captive-bom (multiparous)
Captive-bom (primiparous)
Number of adults
conceiving
N/total
12/13
9/13
12/12
3/5
12/12
3/3
2/4
11/12
5/6
5/5
10/10
4/5
4/6
(%)
(92.3)
(69.2)
(100.0)
(60.0)
(100.0)
(100.0)
(50.0)
(91-7)
(83.3)
(100.0)
(100.0)
(80.0)
(66.7)
Sex of
infants
(M.F.?)
7.5.0
4.4.1
6.6.0
3.0.0
5.7.0
3.0.0
0.1.1
7.4.0
1.4.0
1.0.4
3.7.0
2.2.0
3.1.0
45.41.6
SI
0.2.0
0.0.1
2.0.0
0.1.1
0.0.4
1.0.0
1.0.0
1.0.0
7.1.6
Number of deaths
of infants and juveniles
at various ages (in days)
2-30 31-60
1.0
1.1 0.1
3.2
1.0
0.2
0.1* 0.1*
1.0
1.0 0.1*
1.1 0.1
1.0 1.0
10.7 1.4
23.14.6
61-110
1.0
1.0
1.0
2.1
0.1
5.2
Deaths occured accidentally during handling. These individuals are not included in any subsequent analysis of mortality.
However, no twinning occurred in our captive A. jamaicensis.
The neonate of this species is so large at birth, compared with
the mother, that it is difficult to imagine a female successfully
carrying two young to term.
Most phyllostomids produce two young per year, one at a
time, whereas temperate zone vespertilionids produce single
litters of one to four young. Apparently, the differences in
reproductive strategies are due to temperature fluctuations and
to different temporal patterns of food abundance (Wilson,
1979).
INTERBIRTH INTERVALS.?During their first year in captivity
the reproductive cycles of the NZP bats remained synchronized
with the cycles of the wild population in Panama from which
they were taken. Inclusive birth dates of birth groups BG-I and
TABLE 3-5.?Frequency of conception in the NZP colony of Artibeus
jamaicensis, tabulated by origin and reproductive experience of females in an
r-by-c contingency table. Expected values are in parentheses (Choi, 1978). X2
= 6.62, df= 2,0.02 < P < 0.05.
Origin and
reproductive
experience
of females
Wild-caught
Captive-born
(multiparous)
Captive-bom
(primiparous)
Number Percent
Number of not of females
pregnancies pregnant conceiving
66 (62.5)
12 (12.2)
14 (17.4)
6 (9.5)
2(1.8)
6 (2.6)
91.7
85.7
70.0
BG-I I of the NZP bats corresponded approximately to birth
dates in the free-living Panamanian population (Table 3-4).
However, from BG-III on, births began to occur sooner than
expected, based on the reproductive seasonally of the
free-living Panamanian bats. Delayed embryonic development
should have deferred births in BG-III until February 1980, but
births in the colony began in late November 1979 and were
completed by the end of January 1980. BG-IV was approxi-
mately 1.5 months ahead of the predicted schedule, and BG-V
was more than two months early. If delayed embryonic
TABLE 3-6.?Analysis of sex ratios of neonates in the NZP colony of Artibeus
jamaicensis by birth group and mother's origin.
Grouping
Birth group
BG-I
BG-II
BG-III
BG-IV
BG-V
BG-VI
Totalf
Mother's origin
Wild-caught
Captive-bom
Males (N)
7
4
9
8
9
8
45
32
13
Females (N)
5
4
6
8
8
10
41
33
8
P*
0.1934
0.2734
0.1527
0.1964
0.1855
0.1669
0.0783
0.0978
0.0970
*One-tailed exact binomial probability test.
t BG-I through BG-VI, combined:
df= 12, - 2 sum In P = 19.834 = X2, 0.10 > P > 0.05.
26 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 3-7.?Length of interbirth intervals in the NZP colony of Artibeus jamaicensis.
Interval
between
birth groups
i-n
Il-IIIt
III-IV
iv-vt
V-VI
Number of
individual
females
7
6
14
13
13
Mean interval
in days (range)
134.6(120-153)
162.2(132-184)
131.2(113-158)
190.9 (159-220)
120.2(112-137)
198.29
443.37
372.34
377.74
50.74
Comparison*
X
Yt
X
zt
X
Source
Between
Within
Total
SS
40561.185
13388.740
53949.925
ANOVA (one-way)
df MS
4 10140.296
48
52
F
36.354
P
< 0.001
* Student-Newman-Keuls multiple comparison test Identical letters denote that differences were not
significant at the 5% level.
t Intervals where delayed embryonic development was presumed to have occurred.
tP<0.01.
development occurred in the captive females at approximately
the same time it occurred in free-living females, then the
interbirth intervals between BG-II and BG-III and between
BG-IV and BG-V would be expected to be longer than
interbirth intervals where development proceeded normally.
These data and interbirth intervals for individual females
between consecutive birth groups (Table 3-7) suggest that
delayed embryonic development did occur in the captives but
was of diminished duration. The average interbirth interval for
normal prenatal development would be about 122 days and the
interbirth interval with delayed embryonic development would
be about 213 days according to Fleming's (1971) data for
free-living Panamanian A. jamaicensis.
Differences between intervals presumed to represent normal
gestations were not significantly different from one another in
the NZP bats as revealed by a posteriori testing (Table 3-7).
The presumed delayed intervals, however, were significantly
different from the normal intervals as well as from each other.
The overall trend in the colony's reproductive output was
toward a shortening of the interbirth intervals and earlier onsets
of successive birth groups than expected if the captives had
remained synchronized with the wild population. Of the two
intervals where delayed development was expected, mean
length of the second interval (BG-IV to BG-V) was nearly 30
days longer than that of the first, although BG-V still occurred
approximately three months ahead of the Panamanian cycle.
Loss of some environmental clue, such as day length, may have
impacted the cycle of the captive bats.
Juvenile Mortality
Forty-three babies died before weaning (Table 3-4). Factors
contributing to deaths were as follows (by age groups):
NEONATAL PERIOD (1st day; 14 deaths).?Mortality was the
result of premature birth, still birth, congenital deformation,
and maternal neglect.
PREVOLANT PERIOD (2-30 days of age; 17 deaths).?This
period was characterized by mothers frequently leaving their
infants unattended, or in the company of other young and/or
adults. Mothers were in estrus during the early part of this
period and were frequently pursued by males. A higher than
normal density of males (never less than five adult males) may
have contributed to increased levels of stress in the colony. The
greatest percentage of infant mortality occurred at this time,
possibly due to this stress.
NEWLY VOLANT PERIOD (31-60 days of age; 5 deaths).?
Young were newly volant, but not yet weaned. Initially, they
remained in the roost, exercised their wings and pectoral
muscles, and accompanied their mothers on short flights. If
they were not strong enough for a return flight to a roost area
and could not find a substrate up which they could crawl to a
roost, or a place high enough to initiate another flight, they
would weaken and die unless they were retrieved by their
mothers or discovered by the keepers.
WEANING PERIOD (61-110 days; 7 deaths).?Juveniles were
becoming more independent, weaning was nearing completion,
and the mothers were starting to reject their young by chasing
them from the roost. Transition to subadulthood was beginning.
Preweaning mortality among infants of wild-caught females
was 35.4% (Table 3-8). Much of this mortality was attributable
to two females (F4 and F12) who consistently failed to rear
offspring (seven babies between them for BG-I to BG-VI)
because of congenital defects (e.g., skeletal deformities) or
intestinal ncmatode infestations in the young. These females
were able to rear young successfully beyond weaning age when
they were removed from the colony and placed in a larger flight
NUMBER 511 27
TABLE 3-8.?Correlation of infant and juvenile mortality and level of maternal experience. Numbers of infant
deaths in various age groups are tabulated in an r-by-c contingency table with expected values in parentheses
(Choi, 1978). X1 = 20.697, tf= 4, P < 0.001.
Origin and
reproductive experience
of females
Wild-caught
Captive-born
multiparous
primiparous
Total for colony
Number
of
births
65
10
14
89
Number of deaths
during preweaning
<, 30 days
15(21.91)
3 (3.37)
12 (4.72)
30
31-110 days
8 (7.30)
1 (1.12)
1 (1.57)
10
Number surviving
beyond weaning
110+days
42 (35.79)
6 (5.51)
1 (7.71)
49
Percent
preweaning
mortality
35.4
40.0
92.9
44.9
Percent
postweaning
survival
64.6
60.0
7.1
55.1
TABLE 3-9.?Analysis of mortality among captive-bom bats by sex. Numbers of infant deaths in various age
groups are tabulated in an r-by-c contingency table with expected values shown in parentheses (Choi, 1978). X1
= 5.860, df= 3, 0.25 > P > 0.10.
Sex
Males
Females
Total
Total
births
45
38
83
Total
deaths
23
11
34
<.\
7 (4.34)
1 (3.66)
8
Age in days
2-30
10 (8.67)
6 (7.33)
16
31-110
6 (5.42)
4 (4.58)
10
Survivors
110+
22 (26.57)
27 (22.43)
49
cage with fewer bats. Thus, they may have been in poor
nutritional condition from excess stress or social exclusion
from food, factors that could have affected their offspring's
growth in utero and postpartum development Excluding the
young born to females F4 and F12 would reduce mortality of
juveniles of wild-caught mothers to about 27%.
Preweaning mortality among offspring of multiparous
(experienced) captive-born mothers was 40%, attributable
entirely to the deaths of all young born during BG-VI. We have
no explanation for this catastrophe. In contrast, approximately
64% of the young born to primiparous (inexperienced) females
did not live more than a day, and nearly 86% did not survive a
month. Sixty percent or more of the young of experienced
mothers (wild-caught females and multiparous captive-born
females) survived beyond weaning, but few (7%) of the young
of primiparous females survived that long.
Apparently, preweaning mortality and postweaning survi-
vorship are dependent on the mother's level of reproductive
experience (Table 3-8). Deaths of young were not evenly
distributed between the sexes (Table 3-9). In our colony, males
died at a rate greater than expected and females died at a rate
lower than expected, but the differences were not significant.
Lower conception rates and increased infant mortality
among primiparous captive-born females may be attributable to
a variety of causes. In natural populations, young A. jamaicen-
sis probably are forced to disperse from their natal roost before
birth of the next young, and thus parenting behavior would not
be acquired through learning. Despite proximity to experienced
females at the NZP, inexperience may have operated to increase
mortality of infants born to our captive, primiparous females.
Increased mortality due to inbreeding could also have been
involved, because the inexperienced females could have mated
with their male parent, male siblings, or other related males.
However, the subsequent successful reproduction in these
females suggests that this was not an important factor.
Kleiman (1980) discussed several physiological and behav-
ioral means whereby reproduction may be suppressed in
socially subordinate female mammals in captive situations.
Abortions, stillbirths, inadequate maternal care, and one
apparent case of depressed lactation were the causes of death
for several of the first young born to our captive-reared females.
In Panama and Mexico, groups of 4-11 adult female A.
jamaicensis accompanied by their juvenile offspring and a
single adult male, occupied tree hole roosts, whereas foliage
roosts (palm fronds and subcanopy trees) were occupied by
solitary males or small groups of subadults (Morrison, 1979).
Tree hole roosts probably are preferred over foliage roosts by
reproducing females, as they provide greater protection from
rain, predators, and fluctuations in temperature (see Section 8,
Roosting Behavior). While foraging, female A. jamaicensis
usually leave their young in the roosts (Fenton, 1969).
Trune and Slobodchikoff (1976) found that clustered
Antrozous pallidus were less agitated and had less weight loss,
lower oxygen consumption, smaller body temperature-ambient
28 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
temperature differentials, lost less heat to the environment, and
conserved more metabolic energy while inactive, than bats
roosting individually. Any or all of these factors could be
important to prenatal and postnatal development.
Our captive-born female Artibeus jamaicensis first produced
young while they were still in nonclustering "subgroups." The
implication is that these females were not in the appropriate
social environment (harem) necessary for infant development.
For some free-living populations, tree hole roosts may be
critical resources for reproduction and the cluster of bats within
the roosts may be vital as a source of "helpers" to maintain the
appropriate thermal conditions for the young bats. These
factors might explain the failure of our primiparous captive
females to successfully rear offspring.
Neonatal Physiognomy
Between 29 January 1979 and 30 April 1981, at least 78
full-term bats were born at NZP. Unless otherwise noted in the
descriptions that follow, observations on neonates refer to 37 of
these infants on their first day of life. Neonates were first
examined at the beginning of the dark period and were
probably from 1 to 14 hours old when first seen. All neonates
retained a segment of dried umbilical cord. Frequently, bits of
dried amniotic membrane were present on their bodies as well.
By the second day, the cord and all dried membranes were
gone, except for two infants that still retained umbilical cords.
All neonates had their eyes open, and most had ear pinnae
and noseleaf erect when they were first examined. A few had
the pinnae and the noseleaf flattened against the head, but they
became erect within six hours. Ear openings usually were
apparent and the neonates twitched their pinnae or bodies in
response to sounds. Six babies did not show ear openings or
respond to sounds until as late as four days following birth.
However, all infants examined had the ability to emit ultrasonic
sounds in the 80 kHz range on their first day. A. jamaicensis
emit their ultrasonic orientation calls through the nose (Griffin,
1958), and, accordingly, the mouths of infants were closed
when they produced ultrasonic emissions. Their nostrils and the
grooves at the base of the noseleaf on the outer edges of the
nostrils quivered visibly during such vocalizations.
The neonates usually were covered sparsely with dark gray
fur on the dorsum and top of the head. The ears, muzzle, wings,
and venter were hairless. Nonfurred skin usually was pink.
However, a few neonates had dark gray skin.
The feet of neonates were well developed and disproportion-
ately large. The wings appeared short, narrow, and relatively
less developed compared to the otherwise precocial physical
condition of the neonates. Bones of fingers and joints were soft
and flexible. The bones and skin of the wing tips were
unpigmented and translucent, and the tip of digit III often
curved in toward the body more than 180 degrees.
Average physical measurements of neonates were taken on
22 individuals, each of which survived at least three weeks.
Males and females did not differ significantly in mass, forearm
length, wing span length, or wing area, although average size of
female neonates exceeded that of males (Table 3-10).
Phyllostomid neonates are comparatively large at birth, with
neonate-to-mother mass ratios usually exceeding 0.25 and
forearm ratios exceeding 0.41 (Kleiman and Davis, 1979;
Figures 3-2 and 3-3; Table 3-11). A. jamaicensis compares well
with these observations, with a neonate-to-mother mass ratio of
0.26 and a forearm ratio of 0.54 (Table 3-10).
Neonatal Behavior
Newborn young in the zoo colony typically were found
hanging beside their mothers with mouth grasping one of the
mother's nipples. Young thus attached kept their wings folded
and did not appear to use their thumbs for clinging. Often, a
mother shielded her infant, at least partially, with a wing. It was
rare to find a neonate with its feet also attached to its mother
while resting quietly in the roost. On the other hand, it was not
unusual to find newborn infants hanging alone in the roost.
They hung quietly, with both feet attached to the ceiling, their
wings folded, and often had their eyes closed. They appeared to
be sleeping.
Neonates were able to crawl about in a slow and wobbly
TABLE 3-10.?Body mass and measurements of wings of neonate Artibeus jamaicensis in the NZP colony.
Variable
Mass (g)
Forearm length (mm)
Wing span (mm)
Wing area (cm2)
Wing loading (g/cm2)
Aspect ratio
(wing span2/wing area)
Female, N = 12
mean
14.1
33.9
235.8
77.2
0.187
7.41
SD
2.100
2.749
18.195
18.865
0.025
0.869
Male.W
mean
13.7
33.0
227.5
71.6
0.198
7.49
= 10
SD
1.655
2.088
15.501
17.666
0.034
1.252
Combined,
mean
13.9
33.5
232.0
74.7
0.192
7.45
N = 22
SD
1.878
2.453
17.159
18.120
0.029
1.034
t*
0.513
0.811
1.144
0.715
0.825
0.168
P
ns
ns
ns
ns
ns
ns
Sex
ratio
(F/M)
1.031
1.026
1.036
1.078
0.944
0.990
Percent
adult
size
0.264
0.542
0.504
0.276
1.118
0.942
* Student's /-test for significant differences between the means of males and females (one-tailed).
NUMBER 511 29
1.2-1
HI
i-
<
z
o
w
z
o
o
0.4-
0.4-
D
0.6 1.2 1.8
LOG ADULT MASS (g)
FIGURE 3-2.?The relationship between neonate mass and adult mass for 18
species of bats. Log neonate mass (g) is plotted against log adult mass (g). The
regression line for vespertilionids (solid circles) is y = -0.60 + 0.93 x, (r =
0.942, P < 0.001). Phyllostomid (open triangles) and molossid (open squares)
data points are shown for comparison. Data are from Table 3-11.
fashion and were active in the reattachment process upon
reunion with their mothers. They showed a strong tendency to
keep their heads downward. When a mother was held in a
head-up position, the attached neonate readjusted its position
with its feet until it grasped its mother's head. Turning the
mother head-down caused the baby to resume the normal
head-down posture. Neonates placed on a vertical wire mesh
surface with their heads up immediately started to invert. They
also tended to crawl upward (achieved by "walking" backward
with the feet). Older babies tended to crawl upward until
stopped by an obstacle or lack of a foothold, but neonates
usually crawled upward only a few centimeters and then
stopped.
Autogrooming in A. jamaicensis consists of licking the body
surfaces and raking or scratching body surfaces with one foot
while hanging by the other. Neonates were seen licking
themselves, especially their wing surfaces, but they never hung
by one foot in order to use the other foot to groom.
Allogrooming is known in this species to include the grooming
of infants by their mothers. Occasionally an infant extended a
wing to its mother as if to solicit grooming, and the mother then
licked the baby's wing. Mothers frequently sniffed young other
E
E
HI
CC
o
U_
LJ
<
Z
o
LU
o
o
1.60n
1.25-
Q90-
1.4 1.6 1.8
LOG ADULT FOREARM (mm)
FIGURE 3-3.?The relationship between neonate and adult forearm lengths for
19 species of bats. Log neonate forearm (mm) is plotted against log adult
forearm (mm). The regression line for vespertilionids (solid circles) is y = -0.24
+ 0.88 x, (r = 0.879, P < 0.001). Phyllostomid (open triangles) and molossid
(open squares) data points are shown for comparison. Data are from Table 3-11.
than their own and often huddled with them, but they licked
only their own young. We never observed allogrooming
between adults at the NZP, but it must occur occasionally in
wild adult A. jamaicensis. That would best explain the chewed
necklace bands we noted in some individuals that were
captured on BCI.
When we separated a neonate from its mother's nipple, it
appeared anxious and was quick to restore a holdfast with its
mouth, but it often was not discriminatory about the substrate
it happened to grasp. As they were being examined the
newborns frequently succeeded in biting our fingers, and on
two occasions babies remained attached and began to suck
vigorously. By the second day postpartum, the babies were
more discriminating about what they would grasp with their
mouths. In order to avoid falling, they would bite our Fingers
when prevented from clasping our hands with their thumbs and
hind feet, but none tried to suck the skin. Infants were never
found attached to females other than their own mothers.
Disturbed mothers carried their babies with them in flight.
30 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
?2
Si
I1*
III
PJ
"1 ? ? ^ ? o o ?? grs ^ l -aS^S^^" 0
? -
 2
. "51~. ^ ? 1 - s "- - s" I g f f Z " rf
Q * o ^ o o u : a o ^ ^ S J 2 ^ a : & . S S Q a a a
1 U U U
oo ? O O
d o ? d
en oo
d d
vn vn N w a ?
? oi <j a w vi
<s ? ??
d o o
N N vi CK c^  ?v * c~; p ? ? q ? IN is >n t ^
d o o d d d d o d d d ci ci o d d do
o o o > n o vn ? vi vn vi o O vn o o r ~
?*Q5 v i f S v N ? n <f o N N ^ v n ^
1
1 I 5 a
qvno; q - oo - - j p h <* o ?+ <=> P^C^^S1 ?? <n
^ * )^ c*> O >O c*^  c*> *o f^ ? ^ ^ O ^ ^ ^^ O O O M O O oo
f ^ C J j ^ ? ^ * * t - ^ o^ -^ oe Q oo in v i ^ ? o 6 * r i r s w S ?n ?*
?a
NUMBER 511 31
Apparently the babies instantaneously detached their feet from
the ceiling as the mother spread her wings to take off. When a
mother with a baby attached to one of her nipples was netted in
flight, the infant usually was found in a position parallel to its
mothers's body, its feet gripping her femur or inguinal region.
Rarely, an infant was found in a crosswise posture such as that
noted by Kleiman and Davis (1979) for Carollia perspicillata.
In this case, the infant's feet were attached to the opposite
nipple region and the baby was carried across the mother's
chest just behind her throat.
Growth and Development of Young
GROWTH OF HAIR.?Follicular activity preceding growth of
fur caused the color of the skin to change from the neonatal
pink to gray. Skin of the underparts darkened around seven
days of age, and hair growth began at 12 days. At this time,
young also began to groom themselves with their feet. The
sparse, appressed fur on the head and dorsum was erect and
starting to thicken on day 15. The muzzle area darkened around
day 17, and facial fur growth started about day 20. By day 22
65-i
6 0 -
^ 55-
E
E
o
z
UJ
50H
4 5 -
UJ
? 40-
u.
35-
3 0 J
0 25 50
AGE (days)
75 100
FIGURE 3-4.?Growth of forearm in the NZP colony of Artibeus jamaicensis. Daily means, standard errors, and
ranges are shown.
32 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
the ventrum was covered with sparse fur. The general and
superciliary vibrissae were only red spots about the corners of
the mouth and eyes until day 25, when they began to protrude.
Thereafter, short, soft vibrissae were also evident. Young had
full pelage by 30 days of age and whitish facial stripes were
apparent on some individuals.
BODY SIZE.?Growth curves for the four measured charac-
ters (forearm length, wing span, wing area, and mass) are
presented in Figures 3-4 to 3-7. Daily means, standard errors,
and ranges are shown for 22 young from BG-I and II. Data
derived from deformed or markedly underdeveloped young
that died within a few days of birth were not included in the
computations.
Forearm length showed the greatest development at birth
relative to other measured characters and the fastest growth rate
(X = 0.9 mm/day during the maximum linear growth phase;
Figure 3-4). Forearm growth stabilized around 50 days of age
at X = 61 mm, 1 mm less than the average forearm length of
bats of the original adult colony (Tables 3-1 and 3-12).
Wing span increased by X = 5.8 mm per day and wing area
by X = 3.8 cm2 per day during the maximum growth phase, and
both reached adult proportions in X = 70 days (Figures 3-5 and
3-6). Body mass showed the slowest rate of increase (-0.5 g
per day; Figure 3-7) and took nearly 80 days to stabilize at X
= 48 g, which was 5 g less than the average adult body mass of
500-
E 400-
E
z
Q.
o
z
r 300-
2OOJ
o 25
I
50
AGE (days)
?r-
75 100
FIGURE 3-5.?Growth of wing span in the NZP colony of Artibeus jamaicensis. Means, standard errors, and
ranges are shown.
NUMBER 511 33
TABLE 3-12.?Average asymptotic measurements by sex of Artibeus jamaicensis in the NZP colony.
Variable
Mass (g)
Forearm (mm)
Wing span (mm)
Wing area (cm2)
mean
48.4
61.7
466.7
264.73
Females
SD
3.462
1.377
10.630
18.155
n
20
19
15
7
mean
47.6
60.7
457.1
257.77
Males
SD
2.923
1.635
91.400
8.789
n
18
18
14
6
t*
0.077
2.058
2.600
0.853*
Pi
ns
< 0.025
<0.01
ns
Sex ratio
(F/M)
1.017
1.016
1.021
1.027
* Student's /-test for significant differences between the means.
t One-tailed.
$ The variances for measurements of male and female wing area were not homoscedastic, so a Wilcoxon
two-sample test was also performed (Ut = 25, ns).
300-1
250-
o
A
R
E
A
O
z
200
150
100-
50 J
r
0
[
25
l
50
AGE (days)
75 100
FIGURE 3-6.?Growth of wing area in the NZP colony of Artibeus jamaicensis. Means, standard errors, and
ranges are shown.
34 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
the colony's original members (Tables 3-1 and 3-11).
Sexual dimorphism was not as apparent in the asymptotic
size of the captive-reared young as it was in the wild-caught
bats. Again, females exceeded males in all measured variables,
but the differences were significant only for forearm length and
wing span. The magnitude of the differences between the sexes
was also reduced, and females exceeded males in size by only
2%-3% (Table 3-12). The variable best correlated with age
was mass (r = 0.9387, P < 0.0001; where r is the correlation
coefficient and P is probability). All size variables were highly
correlated with one another. The average asymptotic masses of
19 captive-born young were compared with their neonatal
masses, and a significant relationship was found (r = 0.7097,
t, = 4.1459, P < 0.001; Figure 3-8). Large infants tended to
become large adults.
INFANT-MOTHER SIZE RATIO.?There was a tendency for
larger females to produce large infants (Figure 3-9), but the
relationship was not significant (n = 12; r = 0.552; 0.10 > P >
O)
5 0 -
4 5 -
4 0 -
35 -
30-
25-
2 0 -
15-
1OJ
or 25 50
AGE (days)
75 1OO
FIGURE 3-7.?Growth of mass in the NZP colony of Artibeus jamaicensis. Means, standard errors, and ranges are
shown.
NUMBER 511 35
at
CO
5 50H
o
o 46-
a.
2
>-
< 42-
10 15
NEONATAL MASS (g)
20
FIGURE 3-8.?The relationship between the asymptotic mass of captive-reared young and their neonatal mass.
The equation for the regression line is y = 32.94 + 1.05 x, (r = 0.710, P < 0.001).
1.25-1
v>
<
5
UJ
z
o
UJ
o
o
1.15-
1.05-
1.68 1.70 1.72 1.74 1.76 1.78
LOG FEMALE NON-GRAVID MASS (g)
FIGURE 3-9.?The relationship between neonate and mother mass in the NZP
colony of Artibeus jamaicensis. A mean nongravid mass was determined for
each adult female. Means (solid circles) and ranges (bars) of infant mass are
shown. The equation for the regression line is y = -0.14 + 0.74 x, (r = 0.552,
0.10<P<0.05) .
0.05). However, relative infant size (as a percentage of the
mother's nonpregnant mass) was correlated with the mother's
potential weight-bearing capacity (wing area/nongravid mass).
A positive relationship between relative neonatal mass and
the mother's wing weight-bearing capacity has not been
recorded for any other species of bat. However, Kunz (1974)
noted that female wing size was larger than male wing size in
Eptesicus fuscus in Kansas where the normal litter is one. He
speculated that if there is any selective advantage gained by
large wing size, the degree of sexual dimorphism in E. fuscus
should be even greater in the more eastern states where two is
the usual litter size.
More attention should be paid to species' wing-loading
values and other variables of wing shape and aerodynamic
ability and their relationships to a variety of developmental,
behavioral, physiological, and ecological factors. Wings are
essential for the location, pursuit, and transport of food. Other
potential functions of wings that also could be wing-size
dependent are heat dissipation, evaporative water loss, trans-
port or shielding of young, and behavioral displays.
The mass of a developing fetus must be of particular
significance to those bats that forage while flying. However,
beyond a certain point in relative size, the larger wings
themselves would represent a significant weight load with
much increased drag and would probably be quite difficult to
36 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
move, given a limited muscle mass (Davis, 1969a).
Oddly, in our colony the female with the greatest propor-
tional wing size (F12) produced infants that were among the
smallest in size (both proportionately and absolutely). Of
course, there may be many other reasons why a female would
produce small young.
DENTITION.?Fifteen young from BG-I and BG-VI were
monitored to determine ages when deciduous teeth were lost
and permanent teeth erupted. The deciduous dental formula of
A. jamaicensis is 2/2 1/1 2/2 0 / 0 x 2 = 20. At birth, both
deciduous upper incisors, the upper canine, upper premolar 4,
both lower incisors, and the lower canine projected from the
gingivum. The deciduous incisors were tiny, rounded nubs
barely visible between the canines. Upper and lower deciduous
canines and upper deciduous premolar 4 were sharp, slender,
and recurved. The six functional milk teeth served to grasp the
flesh surrounding the mother's nipple. Great care had to be
taken when removing attached young from nipples as the skin
was easily torn by the teeth.
Patterns of replacement of deciduous teeth were variable.
The upper deciduous first incisors were shed at about 7 days of
age, followed by the eruption of the upper and lower permanent
first incisors. The upper permanent canines began eruption
around 17 days, followed by the lower canines at 21 days. The
deciduous canines were retained about ten more days until the
secondary canines had fully erupted.
The permanent premolars and molars were visible through
the gum from birth and began erupting before canine eruption
was completed. Eruption of teeth in the upper jaw slightly
preceded that of the lower. The unerupted deciduous premolars
sometimes broke through the gum along with their respective
permanent teeth and were lost as eruption was completed. The
second deciduous incisors were the last milk teeth to be shed,
followed by the eruption of the permanent second incisors,
which are small in the adult and probably nonfunctional. The
adult dental formula, 2/2 1/1 2/2 2 / 3 x 2 = 30, was achieved
by 40 ? 6 days.
Compared with vespertilionids, phyllostomids generally
have a milk dentition that is simpler?teeth smaller, reduced in
number, and not so strongly recurved. Kleiman and Davis
(1979) thought this correlated with the phyllostomid's ten-
dency when foraging to carry attached young rather than
depositing them in creches. However, Artibeus jamaicensis
does not often transport its young, and our data from BCI do
not support the idea that phyllostomids in general carry their
young while foraging. Thus, in that regard they resemble many
temperate zone vespertilionids (Davis, 1970; Fenton, 1969).
PATTERNS OF DEVELOPMENT.?Although there are a number
of reports on growth and development in vespertilionids, there
is not enough detailed information on phyllostomids to permit
meaningful comparisons of the two families. It is possible,
however, in search of patterns, to describe trends among the
vespertilionids and then to compare them with the meager data
for the phyllostomids.
1. Development at Birth: Attempts to rank neonatal bats
as altricial, precocial, or intermediate have resulted in classify-
ing phyllostomids as generally precocial and vespertilionids as
comparatively altricial (Gould, 1975; Kleiman and Davis,
1979).
2. Development of Sight: Whether or not the opened eyes
of phyllostomid neonates are functional has not been estab-
lished. If they are, they could be useful in orienting the young
away from illuminated and exposed substrates during day
roosting. A number of phyllostomids roost in exposed locations
such as the undersides of foliage and branches, in rock crevices,
under overhanging roots, under stream banks, and in hollow
logs and abandoned burrows (Tuttle, 1976).
3. Hairiness: Because most tropical phyllostomids,
including A. jamaicensis, have small nursery colonies (Brad-
bury, 1977) or have nursery roosts in exposed locations, it may
be necessary for their neonates to be at least partially furred.
However, two phyllostomids, Vampyrum spectrum (Ditmars,
1936) and Phyllostomus hastatus (Gould, 1975), have hairless
neonates. Vampyrum spectrum, the largest bat in the New
World (180 g), roosts in small groups (<10), in tree holes
(Vehrencamp et al., 1977). Phyllostomus hastatus is the third
largest New World bat (80-120 g). Harems of five to ten
females and a single male roost in hollow logs, hollow trees,
houses, and caves. McCracken and Bradbury (1977, 1981)
found thousands occupying large caves in Trinidad. Because
thermal conductance (heat loss) is negatively correlated with
body size in mammals (Bradley and Deavers, 1980), tempera-
ture stress may be less of a problem for these larger species
(their babies are probably larger as well).
Positive relationships between colony size, ambient cave
temperatures, and enhanced growth rates have been reported in
Myotis grisescens by Tuttle (1975). The large numbers
probably help maintain homeothermy and a high roost
temperature and thus alleviate the need for the newborn to be
furred.
4. Metabolic Rates: Bats show some life history character-
istics that depart from the norm for small mammals. Artibeus
jamaicensis and bats in general are unusually long-lived, have
low intrinsic rates of natural increase, usually have a litter size
of one (maximum recorded litter is five in Lasiurus cinereus),
and show relatively slow prenatal and postnatal development
(see review in Eisenberg, 1981).
5. Brain Size: Most bats that pursue insects on the wing
(e.g., many vespertilionids and molossids) have an Encephali-
zation Quotient (EQ; see Jerison, 1973) that barely exceeds
those shown by many of the Insectivora (Eisenberg, 1981).
Conversely, phyllostomids and pteropodids have brains that are
larger than would be predicted from their body masses (EQ >
1.0). Eisenberg and Wilson (1978) noted that most species in
these families are foraging for rich food resources isolated in
small patches, an activity requiring relatively larger brains to
process and store information.
NUMBER 511
Q2-
37
>?
(0
?D
O)
til
o
cc
O
O
O
"0.6-
"1.4J
D A
A
A
"0.4 0.4 1.2
LOG NEONATE MASS (g)
FIGURE 3-10.?Rates of mass increase versus neonate mass for 18 species of
bats. Log growth rate (g/day) is plotted against log neonate mass (g). The
regression line for vespertilionids (solid circles) is y = -1.09 + 1.14 x, (r =
0.873, P < 0.001). Phyllostomid (open triangles) and molossid (open circles)
data points are shown for comparison. Data are from Table 3-11.
6. Gestation: Eisenberg (1981) showed that among spe-
cies of similar body size, gestation is longer in the species with
a larger adult EQ. Longer gestations and larger brains in
phyllostomids contrast with brief gestations and smaller brains
of most vespertilionids and of other bats that pursue flying
insects. Our data on A. jamaicensis support Eisenberg's
hypothesis.
Duration of undelayed gestation varies in bats from as few as
40 days in insectivores to over 100 days in frugivores. The
estimate of 112 days gestation for A. jamaicensis accords with
the trend suggested by Eisenberg (1981) of extended gestations
in tropical frugivores.
7. Size and Growth Rates: These relationships are best
presented as double logarithmic plots. We used least-squares
regression to calculate the y-intercept (a) and the slope (b) for
the equation: log y = log a + b log x, where x is body mass and
y is the life history variable under investigation.
We examined pairs of variables separately for mass and
forearm length in the vespertilionids (Figures 3-10 and 3-11).
Correlations for both measures between neonate size and adult
size, and between growth rate and either neonate or adult size
are significant Comparable data for molossids are not
sufficient to show trends, but the larger, slower-growing
phyllostomid young appear to depart from the vespertilionid
tendencies.
Q3n
E
~ QO-
a
a
o
_ J
-Q6J
0.90 1.25 1.60
LOG NEONATE FOREARM (mm)
FIGURE 3-11.?Rate of forearm growth versus neonate forearm length for 19
species of bats. Log growth rate (mm/day) is plotted against log neonate
forearm length (mm). The regression line for vespertilionids (solid circles) is y
= -1.56 + 1.29 x, (r = 0.736, P< 0.001). Phyllostomid (open triangles) and
molossid (open squares) data points are shown for comparison. Data are from
Table 3-11.
Development of Wings and Flight
MORPHOMETRICS.?Findley et al. (1972) defined and de-
scribed the probable functional significance of three wing
variables as follows:
1. Wing-loading is the mass (in grams) supported by the
surface area of the wings (in cm2). If the mass-to-wing area
ratio is high, a high speed is necessary to stay airborne. Thus,
rapid fliers will tend to have high wing-loading values, and
slow flight probably requires low wing-loading.
2. Aspect ratio is a measure of relative wing width, and as
calculated by Findley et al. (1972) is wing length divided by
wing width. We calculated it according to Vaughn (1959) the
conventional way as wing span (mm)2/wing area (cm2). High
aspect ratios denote narrow wings and low aspect ratios
indicate broad ones. With high aspect ratios drag is decreased
and greater speed is possible, but lift is reduced. Therefore,
more rapid flight is required to remain aloft. On the other hand,
with low aspect ratios greater lift is possible at low speeds, but
there is more drag at higher speeds.
3. Tip index, a measure of propulsion, is calculated as wing
tip length (length of third digit, mm) divided by length of
38 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
forearm (mm). The wing tip is the main propulsive part of the
wing. Consequently, relatively longer tips are correlated with
greater speed. Hovering species tend to have relatively long
wing tips (hovering is very rapid flight with increased drag to
lessen forward motion).
During the first 40 days of life of our captive bats
wing-loading diminished 26% from near 0.195 to 0.145 g/cm2,
meaning that growth in wing area was proceeding much faster
than growth in body mass. After day 40, wing-loading
increased again to an asymptote of approximately 0.185 g/cm2
(Figure 3-12). Note that the initiation of flight occurred during
the time when wing-loading was minimal. The other aerody-
namic variables (aspect ratio and tip index) were at intermedi-
ate values when young first became volant (Figure 3-12).
Changes in wing shape are shown for a young of known age
(Figure 3-13).
DEVELOPMENT OF FLIGHT.?At first, during drop tests,
infants fell directly to the ground, although most spread their
x
LU
Q
Q.
I-
2CH
1.7-
1.4J
. ? ? ? ?
Q95n
2 0.80-
0.65J
* V '?"?
? ? ? *
m
Q
<
o
-I
o
z
O.2On
0.16-1
0.12J
? ? ?
G
t
F
t
W
0 25 50 75
AGE (days)
100
FIGURE 3-12.?Developmental changes in three aerodynamic parameters of the wings of Artibeus jamaicensis in
the NZP colony. Dots represent daily mean values. Tip index is tip length (mm)/forearm length (mm). Aspect
ratio = wing span (mm)2/wing area (cm2). Wing loading = body mass (g)/wing area (cm2). G = mean age when
young are first capable of gaining altitude and negotiating clumsy landings during drop tests. F = mean age when
young regularly initiate flights. W = mean age of weaning.
NUMBER 511 39
FIGURE 3-13.?Wing outlines from a captive-born Artibeus jamaicensis in the NZP colony. Outlines are actual
tracings of the wing, made when the bat was 2,5, 8,15,23, 30,39,42, 53, and 58 days of age. Flight was initiated
between the 42nd and 53rd days.
wings partially while falling. From day 4 to day 19, the infants
flapped their wings, but still dropped straight down. Around
day 19, the young began beating their wings vigorously, with
full up and down strokes in the roost, but they did not fly. These
stationary wing-beating sessions lasted about 1.5 minutes each,
and there were as many as eight sessions per infant per hour.
Presumably, the function of this behavior was to develop and
condition the muscles necessary for flight. This behavior was
correlated with the last observed transport of offspring by
mothers between different roosting areas. At the same time, the
young also began vigorous scanning in the manner of the
adults, i.e., hanging by one or both feet, with the head upturned,
facing into the center of the flight room, and rapidly moving the
ear pinnae and noseleaf.
By day 24, infants began to achieve some forward motion
when dropped, and they were able to gain some altitude around
day 29. By day 31 they could make clumsy landings on
obstacles. Day 48 was approximately the last day that young
were seen attached to the mother's nipple during the dark
period. We do not know whether infants were attached to the
mother during the light part of the cycle because at that time all
the bats came together into a large clump, in which individuals
were not distinguishable. At this time the young also began to
show interest in the nectar ration that was always available.
They lapped it from food cups and licked droplets off our
fingers. By day 51, young were regularly initiating flights, and
they followed their mothers on flights. They were able to
maneuver and land proficiently by day 65 and thus were
distinguished as "juveniles." The flight skills of juveniles and
subadults were visibly (if not quanu'fiably) distinct from those
of the adults, and at these ages they were much easier to capture
during hand-netting procedures.
Because wings are not essential in the earliest stages of a
young bat's life, it is not unusual to find that the wings are
relatively underdeveloped in newborns. Wing-loading in young
bats and the development of flight abilities have been
investigated in Nycticeius humeralis (Jones, 1967), Antrozous
pallidus (Davis, 1969a), and Myotis thysanodes and M.
lucifugus (O'Farrell and Studier, 1973). As in A. jamaicensis,
initial wing growth was faster than growth in body mass and
resulted in diminishing wing-loading up to the time of flight
initiation. Subsequently, there followed an increase in wing-
loading as body mass increased and the flight abilities were
mastered. We have found no previous reports of vigorous
stationary wing beating for any other bat even though it
probably occurs in most species.
McManus and Nellis (1972) provided an anomalous exam-
ple of ontogeny of wing-loading for A. jamaicensis from the
Virgin Islands. They found an exponential relationship between
log wing-loading (g/cm2) and body mass (g), with larger bats
having progressively higher wing-loading values.
Transition to Subadulthood
The age at which the cartilaginous epiphyseal gap character-
istic of juvenile bats could no longer be detected seemed to be
highly variable in our colony, but this may reflect our
limitations in recognizing precisely the point of closing.
40 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
a.
UJ
a
UJ
o
_l
o
Q5-
UJ
o
oc
UJ
OL
QO-
60 80 100 120 140 160
AGE (days)
FIGURE 3-14.?Age of epiphyseal closure of Artibeus jamaicensis in the NZP
colony. The percentage of young bats (n = 31) showing closed epiphyses is
plotted against age. Mean age of closure was 104 days.
Closure times thought to be reasonably accurate for 31
individuals were averaged. Ages of closure ranged from 70 to
160 days with a mean age of 104.4 days (SD = 19.038, Figure
3-14). More than 80% of the young made the transition from
juvenile to subadulthood between three and four months of age.
Transition to Adulthood
MALES.?In young males, testes were discernable by
palpation at least as early as weaning, when they were 3-4 mm
long. Subsequently, the testes gradually increased to their
maximum size (9-14 mm), which in all cases corresponded to
a time of female postpartum sexual receptivity. In eight of 14
males, sexual activity was initiated during the second birth
group following their own when they were nearly one year old.
The remaining six apparently were capable of mating in the
first group following their own. However, the majority of these
males were born in birth groups where the subsequent interval
to the next birth group was extended due to the occurrence of
delayed development of embryos in the gestating females.
These males were approximately eight months old at the time
of their transition from subadult to adult. Following initial
maximal enlargement, regression of testis size to less than 6.0
mm was not seen.
FEMALES.?Twelve captive females were nearly one year
old at first parturition (X = 332.3 days, SD = 55.178). Assum-
ing a gestation of almost four months, they must have reached
sexual maturity by eight months. Two more females gave birth
at around 18 months, but they may have had undetected
abortions previously.
Preparturient nipple enlargement in captive-born females
was similar to that seen in the original wild-caught females.
The nipples enlarged slightly (from 0.5 to 2.0 mm diameter) at
251 days of age (n = 8, SD = 16.999), which was 84 days
prepartum (n = 8, SD = 20.197). None of the first infants born
to the 14 captive-born females survived more than five days,
and at least six of these infants were probably premature. After
this initial reproductive failure, the nipples in eight females had
regressed to small by 17 days (SD = 10.379) after their infant's
death. Apparently, the nipples of one female had not enlarged
by the time she had given birth.
Five of these females gave birth again, and four of their
young completed weaning. Two females did not show
complete regression of nipples, and the two others had
regressed by 125 and 127 days postpartum. The nipples of the
female whose infant died regressed to small in 23 days.
Summary
Bimodal reproduction and reproductive synchrony occurred
in the captive females as it did in the free-living Panamanian
population from which they came. Reproductive cycles of the
captive bats remained in synchrony with those of the wild
population for the first year, then tended toward shorter
interbirth intervals. Every second birth group showed an
extended gestation period, which we believe was due to
delayed development of the implanted blastocyst, as in the
wild. Duration of normal undelayed gestation was 3.5-4
months. The minimum observed interbirth interval was 112
days (mean 129 days). Mean interval with delayed embryonic
development was 177 days. Maximum weight gain by pregnant
females was 32%. The weight gain adversely affected the flight
abilities of females in late pregnancy. Estrus followed
parturition and peak receptivity was three to four days
postpartum.
Fecundity was depressed in reproductively inexperienced
females but averaged 91% in multiparous females, whether
wild-caught or captive-born. Preweaning mortality was high
(almost 100%) for reproductively inexperienced females and
low for experienced females (35%-40%).
Maximum nipple enlargement, hair loss, and pigmentation
occurred 1.5 weeks prepartum. An increase in the nipple size of
pregnant subadult females was detected four weeks before
fetuses became palpable (ten weeks prepartum). Mean duration
of lactation was 66 days, although it was significantly longer in
females that were gestating dormant embryos (-72 days) than
in those females gestating normally developing embryos (-64
days). Postparturient nipple condition of parous females was
always distinctly different from that of subadults and is,
therefore, useful in assigning females to adult or subadult age
classes.
The neonates were physically and behaviorally precocial.
NUMBER 511 41
Their eyes were open, they had fur on the dorsum, and they
were vocal, responsive to sounds, and very active. They were
large (more than 25% of nongravid female mass, and forearm
lengths exceeded 50% of adult size). The permanent dentition
was complete at 40 days of age.
Developmental rates of captive-born young were quite
variable. Body mass was the measure most highly correlated
with age and stabilized around 80 days of age. Forearm length
increased most rapidly and growth was completed in 50 days.
Wing span and wing area reached adult size in 70 days. Beyond
104 days of age most individuals showed complete epiphyseal
fusion. Initiation of flight in young bats occurred during a
developmental stage when wing-loading values were low
(31-51 days of age).
Reproductive maturity in males, as indicated by testicular
hypertrophy, occurred as early as eight months of age, but more
often by one year of age. Females usually first gave birth when
they were one year old, indicating that they had been sexually
active at about eight months of age.
Significant sexual dimorphism in four wing measurements
(span, area, width, and tip length) was detected in wild-caught
adult captives. Body mass and forearm length were greater in
females than in males, but significance was not demonstrated.
Males had higher wing-loading values than females.

4. Reproduction on Barro Colorado Island
Don E. Wilson, Charles O. Handley, Jr.,
and Alfred L. Gardner
Data on reproduction in bats have accumulated at an
accelerating rate during the past 25 years (Racey, 1982;
Wilson, 1979). Because Artibeus jamaicensis is common and
widespread its reproductive cycle is better known than those of
most other Neotropical bats. However, in-depth studies at a
single locality over long periods, which are essential for
interpreting isolated pieces of information and for elucidating
details of a reproductive cycle, have been lacking.
We augmented our understanding of reproduction in A.
jamaicensis, gained from our colony at the National Zoological
Park (NZP), by gathering information from populations on
Barro Colorado Island (BCI) and vicinity. Our data on
reproduction, accumulated over several annual cycles from
wild-caught bats, demonstrate a high degree of reproductive
synchrony in this species.
In 1971 Fleming presented evidence that embryos of A.
jamaicensis undergo retarded development during part of the
year, and Fleming et al. (1972) demonstrated bimodal polyestry
to be the basic reproductive pattern in this species. Our large
data set from BCI and the adjacent mainland, together with the
results of the study of our NZP colony (see Section 3,
Reproduction in a Captive Colony) provide us the opportunity
to examine this cycle in some detail. We base our outline of the
reproductive cycle of A. jamaicensis on 4447 individual
females captured between 1972 and 1980 on BCI and vicinity.
The Basic Pattern
We confirm the previously postulated pattern of bimodal
polyestry (Fleming et al., 1972; Wilson, 1979), and Fleming's
(1971) statements on delayed embryonic development (Figure
4-1, Table 4-1). In general, females are palpably pregnant in
January and begin to give birth by late February or early March.
They are so synchronized that normally more than half of the
Don E. Wibon, and Charles O. Handley, Jr., National Museum of
Natural History, Smithsonian Institution, Washington, D.C. 20560.
Alfred L. Gardner, NERC, US. Fish and Wildlife Service, National
Museum of Natural History, Washington, D.C. 20560.
population gives birth in those two months. During a
postpartum estrus most of them become pregnant again. This
results in a brief period when individuals are both pregnant and
lactating. Palpably pregnant, but still lactating individuals are
most likely in April, May, or June, between the February-
March and July-August birth peaks.
Young born during the initial birth peak (February and
March) are weaned in April and May. The second cycle of
births commences in July and August with the same pattern of
postpartum estrus and lactation. The young from the second
birth peak are then weaned in September and October. The
difference between the two periods of reproductive activity
occurs when the blastocyst from the second postpartum estrus
implants, but does not develop at the same rate as the preceding
one. The period of delayed embryonic growth covers approxi-
mately three months, and is followed by a period of essentially
normal development during the remaining four.
We were able to recognize individuals that were pregnant
(terminal six weeks), lactating, or postlactating, and as these
events tracked one another over the years of our study, we
recorded peak times for each event. Some variation from year
to year is obvious (Figure 4-1), but the amount of congruence
from one year to the next is striking.
Another way we summarized the data was to combine the
information from all years into a single "average" year (Figure
4-2). Thus summarized and divided into 3-week intervals, these
averages show the bimodal cycle and emphasize the 12-week
diapause between July and November.
Individual Variation
In spite of the great number of marked bats in our sample,
and even though we sampled almost continuously for three
years, we were unable to accumulate a complete record of an
individual female's reproductive history throughout her life-
time. To do so, we would have to capture the same female at
least twice per year during the birth periods. We did catch some
individuals two or more times each year, but not always at
appropriate stages of reproduction. Although our data are not
based on complete individual reproductive histories, it seems
43
44 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 4-1.?Reproductive condition (by week) of adult female Artibeus jamaicensis on BCI, 1975 through 1980.
Week
1975
Total
1976
Total
1977
Total
1978
9
10
11
12
10
11
12
13
41
42
43
44
45
46
47
48
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
1
2
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
24
26
27
No
reproduction
N
12
14
8
1
35
27
3
1
2
16
38
51
9
27
35
28
37
274
0
3
3
2
0
0
1
3
10
5
15
5
1
1
8
33
13
9
7
16
2
1
10
53
21
69
291
101
24
2
4
16
6
4
1
0
5
1
3
5
5
0
0
0
0
0
2
0
1
4
1
%
75.0
87.5
34.8
33.3
51.9
50.0
2.8
5.9
84.2
97.4
89.5
64.3
96.4
92.1
100.0
100.0
0.0
9.4
6.3
15.4
0.0
0.0
14.3
27.3
43.5
45.5
65.2
63.3
25.0
100.0
28.6
51.6
40.6
58.3
53.8
80.0
100.0
50.0
100.0
84.1
55.3
94.5
99.0
70.6
100.0
80.0
66.7
40.0
6.9
4.3
0.0
8.6
1.8
13.6
9.6
17.9
0.0
0.0
0.0
0.0
0.0
40.0
0.0
33.3
18.2
20.0
Pregnant
N
4
2
11
2
19
25
3
35
32
0
0
0
0
0
0
0
0
95
1
19
13
2
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
7
16
2
62
1
9
0
1
8
9
54
21
25
16
20
3
2
1
0
0
0
1
0
0
0
2
7
1
%
25.0
12.5
47.8
66.7
48.1
50.0
97.2
94.1
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
100.0
59.4
27.1
15.4
0.0
0.0
28.6
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
11.1
42.1
2.7
1.0
26.5
0.0
20.0
33.3
60.0
93.1
91.3
78.1
27.6
35.7
13.6
3.8
3.6
0.0
0.0
0.0
12.5
0.0
0.0
0.0
66.7
31.8
20.0
Lactating
N
0
0
4
0
4
0
0
0
0
2
1
6
3
0
1
0
0
13
0
5
14
4
3
1
0
1
6
2
2
0
0
0
3
1
2
0
0
0
0
0
0
1
1
1
47
0
0
0
0
0
0
0
0
7
35
30
14
31
14
10
1
3
0
0
1
0
0
4
0
%
0.0
0.0
17.4
0.0
0.0
0.0
0.0
0.0
10.5
2.6
10.5
21.4
0.0
2.6
0.0
0.0
0.0
15.6
29.2
30.8
42.9
100.0
0.0
9.1
26.1
18.2
8.7
0.0
0.0
0.0
10.7
1.6
6.3
0.0
0.0
0.0
0.0
0.0
0.0
1.6
2.6
1.4
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
21.9
60.3
53.6
63.6
59.6
50.0
55.6
50.0
30.0
0.0
0.0
20.0
0.0
0.0
18.2
0.0
Young
on teat
N
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
4.5
0.0
Pregnant &
lactating
N
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
().()
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
9.1
0.0
Post-
lactating
N
0
0
0
0
0
0
0
0
0
1
0
0
2
1
2
0
0
6
0
5
18
5
4
0
4
7
7
4
6
1
3
0
17
30
17
7
6
4
0
1
0
2
0
1
149
0
1
0
0
0
0
0
1
0
2
5
2
14
8
8
1
7
7
2
2
1
0
4
3
%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
5.3
0.0
0.0
14.3
3.6
5.3
0.0
0.0
0.0
15.6
37.5
38.5
57.1
0.0
57.1
63.6
30.4
36.4
26.1
16.7
75.0
0.0
60.7
46.9
53.1
43.8
46.2
20.0
0.0
50.0
0.0
3.2
0.0
1.4
0.0
2.9
0.0
0.0
0.0
0.0
0.0
4.3
0.0
3.4
8.9
9.1
26.9
28.6
44.4
50.0
70.0
87.5
100.0
40.0
100.0
0.0
18.2
60.0
Total
16
16
23
3
58
52
6
36
34
19
39
57
14
28
38
28
37
388
1
32
48
13
7
1
7
11
23
11
23
6
4
1
28
64
32
16
13
20
2
2
10
63
38
73
549
102
34
2
5
24
15
58
23
32
58
56
22
52
28
18
2
10
8
2
5
1
3
22
5
NUMBER 511 45
TABLE 4-1.?Continued.
Week
28
29
30
31
32
33
43
44
45
46
47
48
49
50
51
52
Total
1979 1
2
3
4
5
7
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
26
29
36
37
38
39
40
41
42
43
44
45
46
47
48
49
'50
51
Total
1980 1
2
3
4
5
6
7
8
9
13
14
15
No
reproduction
N
0
1
3
2
0
1
11
4
14
13
35
16
45
7
21
59
417
28
13
8
2
2
1
8
4
3
3
7
0
4
9
4
1
3
3
4
2
1
2
0
1
12
36
34
26
9
43
36
19
11
90
95
48
5
27
70
1
677
8
59
33
6
3
17
2
17
1
1
10
3
%
0.0
100.0
9.7
100.0
0.0
14.3
91.7
80.0
82.4
86.7
92.1
94.1
95.7
100.0
95.5
98.3
96.6
100.0
29.6
22.2
33.3
33.3
47.1
20.0
3.0
18.8
15.6
0.0
3.8
7.4
6.9
100.0
25.0
25.0
10.5
3.9
3.7
3.7
0.0
9.1
52.2
56.3
72.3
78.8
69.2
74.1
92.7
95.0
100.0
100.0
94.1
98.0
83.3
93.1
98.6
100.0
88.9
96.7
97.1
85.7
75.0
94.4
50.0
63.0
100.0
2.4
8.9
2.2
Pregnant
TV
3
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
185
0
0
19
7
4
2
2
3
4
0
1
0
5
11
7
0
1
5
24
38
18
39
2
1
0
0
0
0
0
0
1
0
0
0
4
1
0
2
0
0
201
1
2
1
1
1
1
2
10
0
1
6
18
%
75.0
0.0
3.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
70.4
77.6
66.7
66.7
11.8
15.0
4.0
0.0
2.2
0.0
4.8
9.1
12.1
0.0
8.3
41.7
63.2
74.5
66.7
72.2
66.7
9.1
0.0
0.0
0.0
0.0
0.0
0.0
2.4
0.0
0.0
0.0
4.0
2.0
0.0
6.9
0.0
0.0
11.1
3.3
2.9
14.3
25.0
5.6
50.0
37.0
0.0
2.4
5.4
13.2
Lactating
N
1
0
16
0
3
4
0
1
0
0
0
0
0
0
0
0
175
0
0
0
0
0
0
6
10
89
12
31
2
63
71
26
0
0
2
7
2
7
13
1
9
6
6
4
3
0
1
0
0
0
0
0
0
1
0
0
0
372
0
0
0
0
0
0
0
0
0
35
82
84
%
25.0
0.0
51.6
0.0
50.0
57.1
0.0
20.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
35.3
50.0
89.9
75.0
68.9
100.0
60.0
58.7
44.8
0.0
0.0
16.7
18.4
3.9
25.9
24.1
33.3
81.8
26.1
9.4
8.5
9.1
0.0
1.7
0.0
0.0
0.0
0.0
0.0
0.0
16.7
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
83.3
73.2
61.8
Young
on teat
N
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
1.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
Pregnant &
lactating
N
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
3
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
3
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
3
0
0
0
0
0
0
0
0
0
0
0
0
%
0.0
0.0
3.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
7.9
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
Post-
lactating
N
0
0
10
0
3
2
1
0
3
2
3
1
2
0
1
1
97
1
0
0
0
0
0
1
3
3
1
6
0
32
30
21
0
8
2
0
9
1
0
0
0
5
22
9
4
4
14
2
1
0
0
2
0
0
0
1
0
182
0
0
0
0
0
0
0
0
0
5
14
31
%
0.0
0.0
32.3
0.0
50.0
28.6
8.3
0.0
17.6
13.3
7.9
5.9
4.3
0.0
4.5
1.7
3.4
0.0
0.0
0.0
0.0
0.0
5.9
15.0
3.0
6.3
13.3
0.0
30.5
24.8
36.2
0.0
66.7
16.7
0.0
17.6
3.7
0.0
0.0
0.0
21.7
34.4
19.1
12.1
30.8
24.1
4.9
5.0
0.0
0.0
2.0
0.0
0.0
0.0
1.4
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
11.9
12.5
22.8
Total
4
1
31
2
6
7
12
5
17
15
38
17
47
7
22
60
878
29
13
27
9
6
3
17
20
99
16
45
2
105
121
58
1
12
12
38
51
27
54
3
11
23
64
47
33
13
58
41
20
11
90
101
49
6
29
71
1
1436
9
61
34
7
4
18
4
27
1
42
112
136
46 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 4-1.?Continued.
weeK
16
18
19
20
21
32
33
34
35
36
37
38
39
40
41
42
43
Total
No
reproduction
N
0
0
9
2
7
8
15
9
13
5
26
36
14
33
59
38
6
440
%
0.0
0.0
32.1
8.3
38.9
61.5
27.3
13.8
23.2
14.3
40.0
64.3
66.7
64.7
73.8
88.4
100.0
Pregnant
N
0
2
1
13
7
0
0
0
0
0
0
0
0
0
0
0
0
67
%
0.0
66.7
3.6
54.2
38.9
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
Lactating
N
2
0
3
7
0
4
36
20
9
8
13
3
1
1
2
0
0
310
%
50.0
0.0
10.7
29.2
0.0
30.8
65.5
30.8
16.1
22.9
20.0
5.4
4.8
2.0
2.5
0.0
0.0
Young
on teat
N
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
Pregnant &
lactating
~N
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
%
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
Post-
lactating
N
2
1
15
2
4
1
4
36
34
22
26
17
6
17
19
5
0
261
%
50.0
33.3
53.6
8.3
22.2
7.7
7.3
55.4
60.7
62.9
40.0
30.4
28.6
33.3
23.8
11.6
0.0
Total
4
3
28
24
18
13
55
65
56
35
65
56
21
51
80
43
6
1078
0)
CO
# ? *
t*
mm
9
o
k .
o
Q.
90 -
8 0 -
7 0 -
60 -
50 -
40 -
3 0 -
2 0 -
1 0 -
1977
\
\
\ n IV '? :
l v
I
t
?
"?
?
?
1978
a
1 *.
l\ ??
\ ? :<-
V"?i /
?' ' hi, \
??
?
1
I
A//
i
5 /
1979 '
I
!\ K 1
? M i 11 T
 !1 1
 1 ?i i i ii '
?' \
? 1!
/ I / M h\
1980
#
n
n
n
11i i
i i
i i
? t1 S A
?r \ I
v V.
?
* ?
*? :
? \ *.\ '.\\\\
10 20 30 40 50 8 18 28 38 48 6 16 26 36 46 4 14 24 34 44
Weeks
FIGURE 4-1.?Percentages of pregnant (solid line), lactating (dashed line), and postlactating (dotted line) female
Artibeus jamaicensis on BCL Each record represents four weeks combined.
NUMBER 511 47
7 0 -
6 0 -
50 H
O
O)
? 40-
c
?
o
S 30H
Q.
2 0 -
1 0 -
Jan Feb Mar Apr May Jun Jiil Aug Sep Oct Nov Dec
FIGURE 4-2.?Average percentage of pregnant Artibeus jamaicensis on BCI (based on data from 1972 through
1980, pooled in three week increments).
clear that not every female takes part in every breeding period.
There are records from each week of the year of females
showing no evidence of reproductive activity (Table 4-1). At
the peak of each reproductive episode, the number of pregnant
females averages about 70% (Figure 4-2).
For females originally banded as juveniles or subadults, we
have 894 capture records in the year following their birth. Of
these, 547 or slightly more than 60% were recorded as
nonreproductive (neither palpably pregnant, lactating, nor
postlactating). From a sample of 1121 capture records of adult
females (individuals that had experienced an earlier preg-
nancy), 449 or 40% were nonreproductive. During any given
sampling period, there are almost always more reproductively
active adults than there are yearlings (Figures 4-3 and 4-4). A
summary graph (Figure 4-5) combining data from 1977
through 1980 shows that yearlings not only breed less
frequently, they are more likely to be out of synchrony with the
reproductively experienced adults.
The Reproductive Cycle
ESTRUS.?Each female has two periods of postpartum estrus
per year. The first occurs immediately following the birth in
February-March; the second immediately following the birth in
July-August. Thus, the estrous cycle is easily controlled by the
timing of parturition except in those females that, for whatever
reason, fail to give birth during a particular reproductive period.
We do not know what physiological and environmental factors
cue estrus at the appropriate time. Perhaps estrus in females that
failed to become pregnant is resynchronized by contact with
48 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
0
O>
(0
*1
9
O
h.
<D
Q .
100-
9 0 -
8 0 -
7 0 -
6 0 -
5 0
40 -
3 0 -
2 0 -
1 0 -
1977
?
i\
i >
i V
i \
i L.
it
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, 1
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1978
J
h
l i
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ft ' l '/ I ' i I
M ' i i
; i
r
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'IfIft
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1979
j.
T '
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i
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1 f I
?A !
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I 1 Ii
\[i \ /' i
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i 1980
i\ / \
' i / \
ft / \
10 20 30 40 50 8 18 28 38 48 6 16 26 36 46 4 14 24 34 44
Weeks
10 20 30 40 50 8 18 28 38 48 6
Weeks
16 26 36 46 4 14 24 34 44
NUMBER 511 49
105
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
FIGURE 4-5.?Average percentages of pregnant yearling (solid line) and older (dashed line) female Artibeus
jamaicensis on BCI, based on data from 1977-1980 combined. Each record represents one week.
adult female roost mates who are following a normal cycle.
COPULATION.?Males have enlarged testes during the
periods when females are undergoing postpartum estrus (see
Section 3, Reproduction in a Captive Colony). The degree of
asynchrony in the system indicates that males may be capable
of inseminating females for relatively long periods overlapping
both birth peaks.
EMBRYONIC DEVELOPMENT.?Fertilization and implanta-
tion follow a normal sequence during each of the reproductive
episodes, but subsequent development differs between the two.
The normal gestation period following implantation during the
first reproductive episode of the year is 3.5-4 months.
FIGURE 4-3 (opposite, top).?Percentages of pregnant yearling (solid line) and
older (dashed line) female Artibeus jamaicensis on BCI. Each record represents
four weeks combined.
FIGURE 4-4 (opposite, bottom).?Percentages of nonreproductive yearling
(solid line) and nonyearling (dashed line) female Artibeus jamaicensis on BCI.
Each record represents four weeks combined.
Implantation during the second episode is followed by delayed
embryonic development, which results in a gestation period of
about seven months (Fleming, 1971). This is a unique feature
of the reproductive cycle of A. jamaicensis. The cues are
unknown, but because the cycle persists when animals are
moved into captivity under environmental conditions unlike
the natural ones (see Section 3, Reproduction in a Captive
Colony), it must be under some genetic control. Eventually, the
synchronization breaks down under constant conditions of
captivity, suggesting that one or more environmental cues are
necessary to reset the system.
PARTURITION.?The two peaks of parturition are in Febru-
ary-March and July-August. The neonates are well-enough
developed to be able to hang by themselves within a few hours
of birth (see Section 3, Reproduction in a Captive Colony).
Only on two occasions did we capture a female with an
attached young. Apparently, the young are left behind shortly
after birth while the females forage.
LACTATION.?Lactation is easily detected and lasts for about
two months (see Section 3, Reproduction in a Captive Colony).
50 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
I | | | I I I | I I I I j l I I I I I I I I I I I ( I I I I I ' I I ' I I ' | ' ' ' ' ' I ' I I I I I
1977 1978 1979 1980
O
CO
O
Q.
50 ?
25-
0 -
25
50 ?
O
(0
O)
o
50
25
0
25
50
50
25
0
25
50
60
40
J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D
1 9 7 7 1978 1979 1980
FIGURE 4-6.?Schematic representation of the reproductive cycle of Artibeus jamaicensis on BCL showing
temporal variation in percentages of pregnant, lactating, and postlactating females. Mean rainfall is shown in the
bar graph at the bottom. Time is in months and years.
Peaks in percentages of lactating females follow about a month
behind the peaks for pregnant females (Figures 4-1 and 4-6).
Lactation in captivity lasts a bit longer in females that are
carrying dormant embryos following the second breeding
episode. This phenomenon can be inferred in our wild
population (Figure 4-6).
POSTLACTATION.?We were able to glean additional infor-
mation about the cycle from individuals we recognized as
postlactating. Apparently there is more individual variation in
the length of time that nipples are classified as postlactating
than in other reproductive criteria (Figures 4-1 and 4-6). Part of
this variation may be an artifact of stages of refinement of our
definition of postlaction. Early in the Bat Project, we presumed
a bat to be postlactating if no milk could be expressed from
nipples although the nipples were large, flabby, and surrounded
by naked skin. Later, the category was expanded to include
females showing new hair growing in around the regressing
nipple, regardless of its size.
NUMBER 511 51
Seasonality, Rainfall, and Abundance of Food
Previous hypotheses (Wilson, 1979) have focused on
energetics as the primary control on reproduction, and this
indeed seems the most logical explanation for the basic pattern
of the cycle in A. jamaicensis. Other factors being equal, one
would expect animals to achieve maximum reproductive output
without sacrificing survivorship of the young.
If we assume that the physiological constraints operating on
an A. jamaicensis result in a litter size of one and a gestation
period of 3.5-4 months, then in a world of abundant energetic
resources, females simply should reproduce continually,
producing up to three young per year. That they do not suggests
that there must be a time when energy sources are in short
supply.
The time of maximum stress might occur at any of several
critical points in the reproductive cycle. Pregnancy, as does
lactation, carries with it an increase in energy demands to
individual females (see Section 2, Physiology; Studier et al.,
1972). Reproductive success should be enhanced if these
stressful periods coincide with periods of peak resource
availability (Bradbury and Vehrencamp, 1977b).
The critical time for most bats is when the young are weaned.
Not only do the growing young have high energy demands,
they are forced to leam to forage at the same time, and
presumably it would be easier to do so when food is readily
available. Readily available food resources also are critical at
the time of weaning in a species showing synchronized
reproductive cycles, because the population size is markedly
increased at that time. There is now a considerable body of
evidence supporting the position that reproductive events in
bats are timed to synchronize with seasonally abundant food
resources (Dinerstein, 1983; Heithaus et al., 1975; Racey,
1982).
Young born in the first reproductive episode (February-
March) are weaned in April-May, and those born in the second
period (July-August) are weaned in September-October. This
pattern is confirmed by our capture records, as the number of
juveniles and subadults increases dramatically during these
periods. On BCI this results in a general pattern in which the
young are weaned during the rainy season (Figure 4-6). If the
bats conceived during the second episode were to develop
normally (in 3.5-4 months), they would be born in November
and weaned at the beginning of the dry season in January.
Foster (1982) has shown that the peaks in fruit availability on
BCI occur in April-May and September-October, with a low
in January at the beginning of the dry season (Figure 4-7).
Therefore, it seems that delayed development has evolved as a
mechanism to avoid weaning young during the dry season
when fruiting trees are scarce. Thus, the reproductive cycle of
A. jamaicensis seems to be an adaptation to the seasonal cycle
of food abundance. Evidence from other localities supports this
hypothesis (Wilson, 1979).
O
<
u.
Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul
FIGURE 4-7.?Schematic representation of seasonality of fruiting activities of canopy trees on BCI. "Activity"
represents the proportion of species that are fruiting (determined by seed traps). Redrawn from Foster (1982, fig.
12).
52 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
Environmental Cues
This unique cycle persisted after the A. jamaicensis were
brought into the laboratory, although it soon began to drift
toward shorter periods of delayed development. This suggests
that in addition to being under genetic control, the bats are
influenced by some environmental cues that reset and maintain
the periodicity of the reproductive cycle each year. Not only
must an environmental cue be detectable by the animals, it also
has to occur at the appropriate time for them to react to the
upcoming period of limited resources. Although the rainfall
pattern probably is responsible for the pattern of fruit
availability, thus providing the evolutionary drive for the
system, it is difficult to see how either rainfall or fruit
availability could serve as proximal cues to trigger the onset of
reproductive episodes.
If the cycle depended entirely on environmental controls
other than photoperiod, we would expect to see slight
variations from year to year, extreme variation in rare years of
unusual environmental fluctuations, and an abrupt change in
the cycle under constant conditions. If the cycle were under
complete genetic control, we would expect to see no annual
variation, persistence of the cycle in unusual climactic years,
and persistence under constant conditions. There are slight
annual variations (Figure 4-1), no data for unusual years
(Figure 4-6), and no abrupt change under constant conditions of
captivity.
In the Old World, an ecologically equivalent species,
Haplonycteris fischeri of the Philippines, has a monestrous
cycle with delayed development (Heideman, 1988). It shows no
annual variation, persistence in unusual climatic years, and a
curious pattern of geographic variation. The persistence lends
support to the hypothesis of genetic control; geographic
variation argues for an environmental component as well
(Heideman, 1988).
Perhaps genetic control is effected through the postpartum
estrus, which essentially sets the time of copulation and
fertilization. In A. jamaicensis, postpartum estrus persists in
captivity, and the period of delayed development diminishes
over time. This would suggest that an appropriate proximal
environmental cue to fine-tune the cycle should be one that
determines the end of the period of delayed development and
the beginning of normal rate of growth of the embryo.
Assuming the 3.5-4 month gestation time seen in the alternate
reproductive period, the critical time would be during
November-December, or the end of the rainy season.
The end of the rainy season is a time of declining food
resources (Figure 4-7) making it unlikely that the proximal cue
to begin normal development of an embryo would be a sudden
change in the amount or kind of energy resource available.
Rainfall itself is an equally poor proximal cue, because the
rainy season does not end abruptly and the amount of annual
variation in daily rainfall at that time of year is greater than the
amount of variation shown by the timing of the first parturition
period 3.5-4 months later.
What, then, is the proximal environmental cue that resets the
cycle on an annual basis? Perhaps variation in night length?
This is one of the more intriguing questions that remain to be
answered about the reproductive cycle of A. jamaicensis and
perhaps other related species that show a similar bimodal
pattern.
Fleming (1988) found a similar bimodal pattern in Carollia
perspicillata in Costa Rica. Although there is no delayed
development, the cycle also persists in captivity. As with A.
jamaicensis on BCI, the cycle is correlated with rainfall
seasonality, and presumably with differential availability of
food resources.
Summary
Artibeus jamaicensis has a unique reproductive pattern
consisting of alternating episodes of normal embryonic
development and delayed development. Individual females
usually produce two young per year, although occasionally
they produce only one. Young females do not give birth in the
calendar year of their birth, but may do so before they are one
year old. Yearlings produce young at a lower rate than do
nonyearlings. The unusual reproductive pattern seems adapted
to take advantage of periods of maximum food availability by
insuring that young are weaned at such energetically favorable
times. The environmental cues responsible for maintaining the
periodicity remain enigmatic, although the persistence of the
pattern in captive animals suggests some measure of genetic
control.
5. Survival and Relative Abundance
Alfred L. Gardner, Charles O. Handley, Jr.,
and Don E. Wilson
Relative Abundance
Artibeus jamaicensis was consistently the most common bat
netted on BCI and adjacent mainland from 1976 to 1980. Its
abundance, however, whether measured on the basis of
absolute numbers or relative to all other species netted did not
appear to follow either a monthly or seasonal pattern. Average
nightly catch of A. jamaicensis per month ranged from less than
five to nearly 80 per netting session and was inconsistent from
month to month throughout the study (Figure 5-1). Because
part of that inconsistency may have resulted from uneven
netting effort from year to year, we examined the capture record
for 1979, the year for which our efforts were the most intense
and for which July and August were the only months we did not
sample. Numbers of A. jamaicensis still showed great
fluctuation from month to month whether measured directly
(averaged on a per night basis) or calculated as a percentage of
total catch (Figures 5-2, 5-3).
We also compared the 1979 record for A. jamaicensis with
that for the five other most common species of frugivorous bats
(Artibeus lituratus, A. phaeotis, Uroderma bilobatum, Chirod-
erma villosum, and Phyllostomus discolor) netted the same
year (Table 5-1; Figure 5-3). If records for February are ignored
as being too few to be useful, A. jamaicensis made up
44%-76% of the nightly catch in 1979 and were caught on 150
of the 151 nights netted. With the exception of A. phaeotis, the
numbers of the other species also fluctuated greatly (Table 5-1):
A. lituratus, 2%-15% (120 nights); U. bilobatum, 1%-15%
(60 nights); C. villosum, 0.5%-7% (39 nights); and P. discolor,
0.2%-7% (40 nights). A. phaeotis (2%-3%; 107 nights)
appears to be relatively evenly dispersed at low density and
most of those caught probably were resident in the vicinity of
the netting station.
We tested the monthly differences in captures of these bats
(Table 5-1) to see if the differences were more apparent than
Alfred L. Gardner, NERC, US. Fish and Wildlife Service, National
Museum of Natural History, Washington, D.C. 20560.
Charles O. Handley, Jr., and Don E. Wilson, National Museum of
Natural History, Smithsonian Institution, Washington, D.C. 20560.
real. The differences proved to be highly significant. Even
when the data for February are removed, overall Chi-square
values are insignificant only for A. phaeotis (X2 = 11.790, df=
9, ns; where df is degrees of freedom and ns means not
significant). The overall Chi-square values are astronomical for
the other five species, even when based on a reduced data set
(minus February; range, 150.926-495.984). For the full set of
data (Table 5-1), numbers of A. jamaicensis are significantly
low (P < 0.001) for January and November, and high (P
< 0.001) for April, June, September, and December.
Unusually high numbers of C. villosum and U. bilobatum
were taken in October and November, and greater numbers of
A. lituratus were caught in November, December, and January
(Table 5-1) than at other times of the year. We reduced the data
set to see what influence the monthly variation in numbers of
the others species may have had on these tests. When the data
for February and all A. lituratus, U. bilobatum, C. villosum, and
P. discolor are removed from the data set (Table 5-1), the
Chi-square values for A. jamaicensis are significantly low for
March (P < 0.01) and May (P < 0.05), and high (P < 0.01) only
for April and December.
The causes of year-to-year variation in population size are
difficult to assess. Annual variations in numbers caught are at
least partly the result of differences in personnel and their
relative experience as well as the evolution of techniques and
capture strategies used from year to year as the study
progressed. Duration of netting episodes, selection of netting
sites, and frequency of nights of netting per month along with
learned net avoidance, undoubtedly were additional contribut-
ing factors.
Numbers of A. jamaicensis, best seen in the October,
November, and December records (Figure 5-1), generally
increased from 1976 to 1980. Captures of A. jamaicensis
tended to be highest when young are first volant (April-June
and September-October) and lowest when the population is
composed mostly of subadults and adults. We do not know how
much of this variation resulted from adverse conditioning due
to having been caught before.
Occasional unusual concentrations of bats at certain fruiting
trees also distorted the monthly averages and percentages of
53
54 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
t-? CS ? O
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NUMBER 511
80-|
70-
O 60 -
O 50 H
>-. 40-1
55
? X
20-
10-
^ 1976
H 1977
? 1978
1980
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
1976-1980
FIGURE 5-1.?Mean nightly catch of Ariibe us jarnaicens is on BCI and adjacent mainland per month from October
1976 through October 1980.
120-.
[?j AH Species of Bats
I Artibeus jamaicensis
C I Artibeus llturatus
JAN FEB MAR APR MAY JUN JUL
1979
AUG SEP OCT NOV DEC
FIGURE 5-2.?Mean nightly catch of all bats caught on BCI and adjacent mainland per month during 1979 and
the mean nightly catch of Artibeus jamaicensis and A. liiuratus during the same period. Figures above bars are
monthly catch of all bats.
56 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
UArtibeus jamaicensis
pj? Artibeus lituratus
MX Uroderma bllobatum
H U. bilobatum & Chiroderma villosum
["I All other
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
1 9 7 9
FIGURE 5-3.?Monthly composition of the bat fauna caught on BCI and the adjacent mainland during 1979. Bars
represent percentages of total catch.
bats captured. The night of 25-26 October 1979 produced 282
bats of 16 species. Only 86 were A. jamaicensis, however;
Uroderma bilobatum (115) was the most numerous species and
Chiroderma villosum (50) was third. Another night with an
unusually high catch was that of 23-24 April 1979. We
handled 255 bats comprising 13 species of which A. jamaicen-
sis numbered 215, including 100 previously unmarked juve-
niles and 53 adult females. Only 40 of the adult females could
have been the mothers of these juveniles (the other adult
females were either pregnant or nonreproductive). This
suggests the possibility of net avoidance, because if first-flying
juveniles are flying with their mothers, as seems a reasonable
yet unproven assumption, then the mothers of 60 were active in
the vicinity, but not caught.
Recapture Frequency
The entire sample of A. jamaicensis marked between
October 1976 and June 1980, consisted of 8907 bats captured
a total of 15,728 times (Figure 5-4, Table 5-2). Fifty-seven
percent (5061 individuals) were caught only once, leaving 3846
captured two or more times (6821 records; Table 5-2, line B).
The number of subsequent capture records per bat diminished
until we were left with a single individual captured 11 times.
From these data we calculated the mean number of captures
per A. jamaicensis (Table 5-2, line C) in each capture
cohort-for the whole sample, for two or more captures, for
three or more captures, and so on. The 8907 bats, captured a
total of 15,728 times, averaged 1.77 captures per individual
(Table 5-2). The next cohort, those captured two or more times,
also has a mean of 1.77 captures per individual. The individual
capture rates of the first five groups (one or more captures
through five or more captures) vary little (1.76-1.77). The
capture rates, however, for each of the remaining capture
cohorts are lower (1.43-1.65, Table 5-2) and more variable.
When the data for the first five capture cohorts are summed and
the derived mean capture rate (1.77) is contrasted with the mean
capture rate for the remaining six cohorts (1.573, data from
Table 5-2), the differences are significant (t = 6.752, df = 8,
P< 0.001).
We used the derived mean number of captures per individual
for one to five captures (1.77) and for six or more captures
(1.57) to estimate the expected numbers (Table 5-2, line D) in
each capture cohort. In most cohorts the actual capture rate is
close to the expected rate. Individuals disappear and recapture
records diminished in our sample at a nearly constant rate
through the first five times a bat is captured. The probability of
recapturing a bat is roughly the same regardless of the number
of previous captures. Therefore, emigration, necklace loss,
mortality rates, and other factors contributing to the disappear-
ance of bats must be nearly constant.
Another illustration of the relationship between successive
NUMBER 511 57
60-
55-
50"
45"
40-
Z 35-
LJ
O 30 J
E
UJ 2 5 -
Q.
15
10-
5"
INDIVIDUALS
RECORDS
% OF RECORDS
1
5061
8907
57
2
2163
3846
25
3
949
1683
11
4
417
734
5
5
171
317
2
6
81
146
1
7
44
65
0.4
8
15
21
0.1
9
4
6
0.04
10
1
2
0.01
11
1
1
0.01
Total
8907
15728
8907
RECAPTURE RATE |Q432|0L438|o>t36|cU32}o><61|Q445|a323|0^86ta333
4 5 6 7 8
NUMBER OF TIMES CAPTURED
i
10 11
FIGURE 5-4.?Recapture curve, recapture rate (rate of decrease), and frequency of capture of Artibeus jamaicensis
on BCI and adjacent mainland between 1976 and 1980.
capture groups is the rate (percentage) of decrease between
adjacent groups (Figure 5-4). This we calculated by dividing
the number of records in a capture group by the number of
records in the preceding group. The rate of decrease (Figure
5-4) is relatively constant up to seven captures (range,
0.432-0.461), but more variable thereafter (range, 0.286-
0.500).
Observed Survivorship
To study survivorship of A. jamaicensis marked from 1976
through 1980, we divided calendar years into half years:
January-June = "spring" and July-December = "fall." Bats
caught and marked as juveniles were assumed to have been
born in the half year in which they were caught. On BCI and
vicinity most births occur between the 8th and 16th week and
between the 25th and 33rd week of each year. Bats first caught
and marked as subadults were assumed to have been born in the
previous half year. We derived a conservative estimate of
survivorship by dividing the number of juveniles, subadults, or
adults marked in a half year into the number in that birth-cohort
sample known to be alive based on the total recapture record up
to October 1980. Bats marked later in the study (especially
adults and subadults marked in 1979 and 1980) had depressed
survivorship rates because of the lack of sufficient time to
accumulate a more complete recapture record. The data
reported on here only cover a span of 4.5 years, but we know
from Wilson and Tyson (1970) of a 7-year-old A. jamaicensis,
and Handley caught two bats after 1980 that were at least nine
years old.
Survival to the first half year after being marked varied
among year-and-age cohorts from a low of 8% for adult
females marked in the spring of 1980 to a high of 58% for
juvenile females marked in the spring of 1978 (Figure 5-5,
Tables 5-3 to 5-8). Other factors in addition to the lack of
sufficient time to accumulate recapture records influenced
survival estimates. One of the more important was the lower
probability of recapturing bats from the channel markers
(Buena Vista and Pena Blanca) and from the four mainland
sites (Bohio, Frijoles Road, Gigante, and Mona Grita Point)
because these bats normally ranged outside of the area we
routinely sampled. These sites were not netted on a regular
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62 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
LU
>
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ffi
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40-r
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20
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A=cf Spring ? = 9
A=cf Fall O= 9 Fall
a
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8
HALF YEARS AFTER MARK
FIGURE 5-5.?Comparison of survivorship of seasonal cohorts of Artibeus jamaicensis marked on BCI and
adjacent mainland from 1976 to 1980; a = adults, b = subadults, and c = juveniles.
NUMBER 511 63
basis and, although producing important information on
movements, these bats did not form a major part of the main
population we were studying. When the A. jamaicensis from
these off-island sites and their recapture records are removed
from the data (presented in Table 5-9), thereby restricting the
analysis to bats marked on BCI and Orchid Island, survival
estimates are higher and vary from a low of 17% for adult males
marked in the first half 1980 to a high of 71% for juvenile
females marked in the spring of 1978 (data from Table 5-10).
JUVENILES.?Overall survivorship into the second half year
of life by juvenile A. jamaicensis was 31% (Figure 5-6, Tables
5-3 and 5-4). Survivorship of juveniles ranged from 25% for
males marked in the falls of 1977 and 1979 to 57% for females
marked in the spring of 1978 (Table 5-3). Survivorship from
combined data from the fall of 1977 to the spring of 1980
suggests that approximately 68% of the juvenile cohort is lost
by the time juveniles enter their second half year (Tables 5-3,
and 5-4). We had anticipated high mortality during the first six
months of life based on studies of temperate-zone bats
(Brenner, 1968; Davis, 1967; Foster et at , 1978; Humphrey
and Cope, 1970,1976, 1977; Keen and Hitchcock, 1980; Mills
et al., 1975; Pearson et al., 1952; Stevenson and Tuttle, 1981;
Tuttle and Stevenson, 1982). Survivorship from the second to
sixth half year after marking among bats marked as juveniles
averages lower than that of adults and subadults (Figure 5-6).
Dispersal during the first year of life is the most likely
explanation for this higher observed "mortality" or disappear-
ance rate. Nevertheless, factors such as death, learned net
avoidance, and loss of necklace (which renders the individual
unrecognizable), as well as dispersal away from the area of our
study, contribute to the disappearance of these bats. Survivor-
ship by the end of the second half year of life (second half year
after mark) averaged 17% (Figure 5-6, Tables 5-3 and 5-4).
Thereafter, the rate of decline parallels that of subadults and
adults.
Necklace loss may be greater in juveniles because we had to
fit bats of this age class with adult-size necklaces. However,
necklace loss cannot explain the more rapid decline in the
second half year of life by which time the bats have attained
near adult size. Survivorship by the end of the second half year
of life (second half year after mark) averaged 17% (Figure 5-6,
Tables 5-3 and 5-4). Thereafter, the rate of decline parallels that
of subadults and adults.
We examined the number of bats caught in each half year
versus the number known to be alive in that half year (Figure
5-7, Table 5-11) to understand the probable causes for the more
rapid decline from the first to second half year of life in
juveniles. The consistently higher percentage of males caught
of those known to be alive in the first half year after being
marked reflects an initially higher recapture rate among males
a
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Artibeus jamaicensis
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A= Subadults
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O
2 3 4 5 6
HALF YEARS AFTER MARK
8
FIGURE 5-6.?Survivorship curves of the three age classes of Artibeus jamaicensis marked on BCI and adjacent
mainland from 1976 to 1980.
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
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NUMBER 511 65
LU
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80-
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F S F S F
1977 1978 1979
o ?
F F S F S
1976 1977 1978 1979
FIGURE 5-7.?Comparison of numbers of Artibeus jamaicensis marked on BCI and adjacent mainland and
recaptured in the first and second half years after mark. Values plotted are recaptures expresssed as percentages
of the numbers known to be alive in the same half year, open circles = females, closed circles = males. Adults,
(a) first half year and (b) second half year of life; subadults, (c) first half year and (d) second half year of life; and
juveniles, (e) first half year and (f) second half year of life.
66 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
(more recaptures within a shorter time). The same pattern
among subadults (Table 5-12) and adults (Table 5-13) for the
half year following their being marked suggests behavioral
differences between the sexes that in turn increases susceptibil-
ity to recapture among males. The pattern is similar among the
three age classes for the second half year after mark, except that
the relationship is reversed for juveniles in the fall of 1977 and
the spring of 1978, and for subadults in the fall of 1978.
Thereafter, there is no pattern emphasizing greater catchability
of males.
Juveniles of either sex marked in their first half year of life
are known to be alive in the second half year in about equal
numbers (Tables 5-3 and 5-4; 30% for males versus 32% for
females). Nevertheless, by the third and fourth half years, the
survivorship rate is higher in females (21% versus 14%, X2 =
13.383, P < 0.01, for third half year; 14% versus 9%, X2 =
9.159, P < 0.02), suggesting either greater mortality in males,
differential emigration, or both, along with possible learned net
avoidance resulting from higher actual recapture rate during the
first year after mark.
Chi-square analysis of bats marked as juveniles showed
some significant differences in survivorship correlated with sex
and season of birth. In general, females have higher survival
rates than males. Spring newborn of both sexes survive better
into the second half year of life than do fall newborn with the
difference between season of birth for females significant at the
0.05 level (35% versus 28%, respectively; X2 = 6.103). In
subsequent half years, the survival rate is similar regardless of
birth season. Spring-born young may have the advantages of
long gestation (seven months versus four), birth in the dry
season, weaning at the beginning of the wet season, and
attainment of subadult age (and near adult size) by the time of
fig scarcity at the height of the rains. Fall-born young, the
product of a short (4-month) gestation period, are born in the
wet season, weaned at the height of the rains when ripe figs are
beginning to be scarce, and become subadults in the dry season.
Preweaning events such as length of gestation and coinci-
dence of birth with wet or dry seasons, may have little effect on
survival of baby bats. Postweaning conditions, however, when
young bats are on their own for the first time, may be critical.
Fall-born bats are weaned in the season of heaviest rains when
there is a greater probability of getting wet while foraging. The
likelihood of getting wet is increased by the scarcity of figs
because there is more reason to fly in the rain if quality food is
harder to find. Wetting and consequent chilling could be fatal
for weanling A. jamaicensis because of their restrictive,
relatively inflexible energy budget (see Section 2, Physiology).
Survivorship to the second half year (first half year after
mark) is not significantly different for males and females
marked as juveniles. However, females appear to survive at a
higher rate by the third and fourth year (P < 0.01 and P < 0.02,
respectively; based on data in Tables 5-3 and 5-4). Survival in
the third half year (second half year after mark) favored
fall-born females over fall-born males (P < 0.05). Reasons for
these differential survival rates are unclear. The higher initial
recapture rate characteristic of males and their higher subse-
quent attenuation rate in the population are both reflected in
these rates. Nevertheless, we can not be sure how much of the
apparent attenuation rate actually reflects greater differential
emigration by males (higher probability of continued residency
by females) instead of mortality.
SUBADULTS.?Speculation on survival and recapture rates of
bats marked as subadults must include the assumption that
these bats are already in the second half year when first
captured. Bats marked as subadults in the fall were born the
previous spring, and those marked in the spring were born the
previous fall. Therefore, the first half year after being marked is
the third half year after birth. Any comparisons of these records
with those of juveniles are on this basis.
There is some unavoidable "slop" in aging subadults.
Subadults caught late in the fall include all individuals born in
the previous spring and some born early in the fall. In the first
weeks of spring the pool of subadults includes all young of the
previous year, and should be at its largest. Midway through
spring the pool should have diminished to its lowest level
because most have become adults (reproductive) regardless of
age. Later in the spring, juveniles of that spring begin to cross
the threshold to subadulthood. However, numbers of subadults
marked in the fall greatly exceed the number marked in the
spring (Tables 5-5, 5-6, and 5-9). This is simply because in a
year-round capture program, most of the subadults are captured
and marked in the fall, leaving fewer unmarked bats to be
captured in the spring. Bats are aged as juveniles only on the
basis of open epiphyses of the metacarpals and phalanges of the
wings. Transition from juvenile to subadult status (ossification
of the epiphyses in the wing) is relatively rapid (see Section 3,
Reproduction in a Captive Colony).
Assuming that subadults already are in their second half year
when first captured, survival rate is slightly higher than in
juveniles (Figure 5-6). Nevertheless, the proportional loss from
the population of the cohort marked as juveniles through the
second half year after marking must have already been
absorbed by the cohort marked as subadults when these bats
complete the first half year after having been marked. Reasons
for that loss are the same as those outlined for losses among
bats marked as juveniles, except that necklace loss may not be
as important a factor.
Observed overall survivorship through the first half year
after mark (34%) for subadults was not significantly different
from that for juveniles (32%, X2 = 3.225), whereas recapture
rate for the second half year after mark was significantly lower
(17% versus 2 3 % , ^ = 22.300, P < 0.001) for juveniles (Tables
5-3 and 5-5). The highest survival rate for bats marked as
subadults was 43% in the fall of 1978 (males, 45%; females,
39%; Table 5-9). As we suggested for our survivorship data on
juveniles, the survival rate for subadults is undoubtedly higher
than the 43% we recorded during the seven half-year periods in
which we accumulated survivorship data. If we restrict our data
NUMBER 511 67
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68 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
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NUMBER 511 69
to bats marked on BCI (including Orchid Island), highest
survival rates for A. jamaicensis marked as subadults are for
bats marked in the spring of 1979 (males, 48%; females, 41%;
Table 5-10). Conservative cumulative survivorship values also
reflect the progressively shorter time we had from which to
record a survivor as this phase of the project neared its end. The
proportion of implied "mortality" resulting from emigration is
unknown, but may be offset by immigration from other
populations.
ADULTS.?Survival among adults parallelled that of suba-
dults (Figure 5-6, Tables 5-7 and 5-8). Observed overall
survivorship through the first half year after mark (30%) for
adults was not significantly different from that for juveniles
(32%) or subadults (34%, X2 = 3.225), whereas survival for the
second half year after mark was the same as that for subadults,
but significantly higher (23% versus 17%, X2 = 22.300, P
< 0.001) than that for juveniles (Figure 5-6; Tables 5-3, 5-5,
and 5-8). The highest survival rate for bats marked as adults
was 43% in the fall of 1977 (males, 41%; females, 45%; Tables
5-7, 5-8, and 5-9). As suggested for our survivorship data on
juveniles and subadults, the survival rate for adults is
undoubtedly higher than the 43% we recorded. If we restrict
our data to bats marked on BCI (including Orchid Island),
highest survival rates for A. jamaicensis marked as adults are
for bats marked in the fall of 1976 (males, 39%; females, 49%;
Table 5-10). However, survival estimates based only on bats
marked in the fall of 1976 are not comparable to estimates from
other half years because the numbers of bats known to be alive
accrued from the second half year after mark (fall 1977) instead
of from the first half year as in all other periods.
Adults as an age group are much more heterogeneous in
actual age than are either subadults or juveniles. Nevertheless,
the attenuation rate of adults closely traced the survival curve
for subadults (Figure 5-6) and indicates that the factors
contributing to losses act similarly in kind and degree on A.
jamaicensis marked as either subadults or adults. The only
factor distinguishing the survival rates of adults from those of
the other age cohorts is the higher rate of loss of males from the
marked sample.
GENERAL OBSERVATIONS.?Thus far in this section we have
concentrated on examining our mark and recapture record to
extract information of possible demographic interest, except for
estimating the size of the bat population on BCI (see Section 6,
Population Estimates). Our survival estimates are based on the
numbers known to be alive as determined from the entire
capture-recapture record. To better estimate actual survival
would require a longer mark and recapture record, and would
require that estimates for necklace loss, net avoidance, and
emigration be factored into the results.
Although we have used the term survival when discussing
recaptures and relative abundance, we acknowledge our
sometimes loose interpretation of the word. There are other
terms, such as "residency," that we could have used. However,
even that seemingly appropriate term has its drawbacks,
because we have been unable to adequately measure site
fidelity and can not distinguish between and among the
possible resident and visitor (or vagrant) categories of bats.
Also, we do not know how far an A. jamaicensis, belonging to
any of these residency categories, will travel to visit a fruiting
tree (see Section 7, Movements).
Our information on necklace loss is based on 5 of 73 (6.8%)
A. jamaicensis that were double banded (necklace and
wingband) and subsequently recaptured without a necklace.
These bats had been wing-banded before 1975 and, therefore,
were all adults when necklaced. Some loss occurs when the
bats are being removed from the net and the necklace slips over
the head after becoming caught in the mesh. We do not know
what other circumstances contribute to necklace loss. Although
lacking supportive evidence, we suspect that loss is higher for
bats marked as juveniles because we must apply necklaces that
fit adults. The looser necklaces could be more easily slipped
over the head of juveniles if this is the usual means for necklace
loss. Fleming (1988) reported a low rate of necklace loss
(6.5%) in Carollia perspicillata and said that losses sometimes
occurred several years after marking.
Frequency of capture seems to have less to do with age than
with sex. The two A. jamaicensis captured most often were
males. Out of 8907 individuals marked between October 1976
and June 1980, only one was captured 11 times, and another
was captured ten times. The male with ten captures was marked
as a juvenile and recaptured three times in the next four months
as a subadult, and six times in the next 14 months as an adult.
Its age when last caught was just under two years. The bat with
11 captures was marked as a subadult, recaptured four months
later as a subadult, and then nine times in the next 14 months as
an adult. At last capture it also was about two years old. Of the
four captured nine times each (Figure 5-4, Table 5-2), one was
a female and three were males. Although approximately equal
numbers of males and females were caught five or more times,
males had consistantly shorter overall capture records. Only 13
males with five or more captures had records of 30 or more
months between mark and last recapture, and only one of these
exceeded 40 months. However, 35 females had full capture
records of 30 or more months and ten had records exceeding 40
months.
We believe that most bats are easier to capture the first time
than subsequently, regardless of age. The frequency-of-capture
curve (Figure 5-4) is steep at first: 57% caught once, 25%
caught only twice, and thereafter levels out. The remaining
18% (1683 bats) were recaptured two or more times (2975
records; recapture rate averaged 1.77). The survival curves for
each age cohort (Figure 5-6) is similarly steep at first and
thereafter levels out.
Sex Ratio
Our sample of almost 17,000 records of A. jamaicensis
shows that both adult and subadult females outnumber adult
70 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
and subadult males 55:45, while juvenile females are
outnumbered by juvenile males 4 8 : 52 (Table 5-14). The
recapture histories of bats marked as juveniles also support the
contention that females have higher survival (or residency)
potential than males (Tables 5-3 and 5-4). The differences,
however, are not significantly different from an even sex ratio
(X2 = 5.25; P = 0.02).
To determine if there was seasonal variation in sex ratios we
organized our data (Table 5-14) into half years with January-
June representing the dry season (three half years) and
July-December representing the wet season (five half years).
In the adult sample (n = 7594), females were in the majority in
every half year. In the subadult sample (n = 4856) females
predominated in six of the eight half years. Males predominated
in two of the three dry seasons in the sample. Among juveniles
(n = 4516) more males than females were caught during the wet
season. Although not statistically significant (X2 = 1.13; P =
0.29), ratios favored juvenile females during two of the dry
seasons and were equal in the third.
We obtained a different subset of sex-ratio data from
roostlings in the two canal-marker roosts we sampled at Buena
Vista and Pefia Blanca. Young large enough to mark, but
probably still nursing, totaled 45. Females outnumbered males
26 : 19 (58% : 42%), not far off of the 55 : 45 ratio seen in
mist-netted adults and subadults, but the near converse of the
48 : 52 ratio found among mist-netted juveniles. A possible
explanation is that juvenile males may leave or be ejected from
the maternity roost earlier than female offspring. Judging from
the observation that we seldom recaptured bats in the roost
where they were marked as juveniles, we believe that all young
of both sexes must disperse before they reach adulthood.
Subadult sex ratio in the roosts was 27 : 1. None of the 27
subadult females had a previous history in either canal-marker
roost.
Age
If most of the adult females produce two young per year, and
if adults and young are equally catchable, then the number of
nonadults in our mist-netted sample in any year should
approach twice the number of adult females. Only in 1979 did
we have a high level of effort distributed fairly evenly through
the year (Table 5-15). In 1979, all captures of adult A.
jamaicensis totaled 2609 (Table 5-16). This translates to 1435
females (2609 x 0.55) and the prospect of 2870 young (1435 x
2). Our actual catch of juvenile and subadult A. jamaicensis for
the year was 2891. In spite of poor distribution of catch effort
during some years, the proportion of young to adult females in
three of the five years was reasonably close to 2 : 1 (3 : 1 in the
other two years).
To determine actual distribution of age in the population of
A. jamaicensis on BCI and vicinity (Figure 5-8) we looked at a
small subset (n = 225) that had been marked as juveniles or
subadults and recaptured at least four times. Among these
known-age bats, the mean age at last capture was 2.02 yrs in the
females (n = 110) and 1.65 yrs in the males (n = 115). The
average for the whole sample (n = 225) was 1.83 yrs. Of the 115
males in the sample, 91 were two years old or less at last
capture and only 24 were more than two years old. Fifty-nine of
the females were two years old or less at last capture and 51
were more than two years old. The oldest male was four and the
oldest female was 6.5 years old.
Mortality
With potentially great longevity, and with most female A.
jamaicensis producing two young each year, the species must
be under severe population controls. Death rate must be high,
but its causes are speculative. Mortality factors include
starvation, predation, accidents, and disease, but we have little
direct evidence and we have seen few dead bats.
INFANT MORTALITY.?Because of our study methods, we
have no direct information on preflight mortality in wild bats.
Most deaths in our NZP colony occurred in the preflight
interval. On BCI we sometimes captured numbers of postlac-
tating females along with lactating bats when few or no
juveniles were caught. This could be explained in part as a
function of natal and postnatal mortality.
Our capture of only ten juveniles among 152 A. jamaicensis
on 11 and 12 April 1979 is a typical example. The condition of
the adult females was 38 lactating, 22 postlactating, five
pregnant, and two lacking evidence of reproductive activity.
We suspect that the postlactating females were primiparous and
that their lack of success in rearing young (hence the
postlactating condition) paralleled the situation found among
first-time mothers in our NZP colony, but this is not supported
by the record. For those postlactating females whose capture
record is sufficient, the majority had been neither juveniles nor
subadults during the previous half year. We do not know if the
inevitable loss of young by primiparous mothers recorded in
the NZP colony was an artifact of their captive environment or
also occurs in natural populations.
STARVATION.?Young of the spring are weaned in a season
of abundant food (April-June) at the beginning of the rainy
season. Young of the second birth group (summer), on the other
hand, are weaned in a season of food scarcity (August-
October) in the middle of the rainy season when they could
easily starve before becoming efficient foragers.
According to Eisenberg and Wilson (1978), it may be more
difficult for frugivorous bats to find enough food than it is for
insect eaters. This would correlate with a relatively large brain
in fruit eaters. Frugivores rely on a food source that is strongly
pulsed in time and space. Their behavior and the nature of their
diet adds risk because fruit-eating bats often congregate in large
numbers at food sources where predators may be attracted and
wait for prey (Howe, 1979; Morrison, 1978a). These bats also
have to search out food sources for the future while still
harvesting a current source (Morrison, 1978b). In contrast,
NUMBER 511 71
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72 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 5-16.?Profile of ages of Artibeus jamaicensis captured on BCI between October 1976 and October 1980.
Age
1976
adult
subadult
juvenile
Total
1977
adult
subadult
juvenile
Total
1978
adult
subadult
juvenile
Total
1979
adult
subadult
juvenile
Total
1980
adult
subadult
juvenile
Total
Number
marked
329
400
162
891
665
658
497
1820
682
746
281
1709
962
748
1285
2995
503
568
1705
2776
Percent
of total
marked
37
45
18
37
36
27
40
44
16
32
25
43
18
21
61
Number
recaptured
57
52
9
118
456
258
35
749
971
281
9
1261
1647
625
233
2505
1322
520
300
2142
Percent
of total
recaptures
48
44
8
61
34
5
77
22
1
66
25
9
62
24
14
Total
captures
386
452
171
1009
1121
916
532
2569
1653
1027
290
2970
2609
1373
1518
5500
1825
1088
2005
4918
Percent
of total
captures
38
45
17
44
36
21
56
34
10
47
25
28
37
22
41
most insectivorous bats harvest a fairly static resource while
flying a stereotyped, generally solitary search pattern.
Young A. jamaicensis have much to learn when trying to
find enough to eat. For young females this may be less
traumatic, for they probably stay for a longer time in the natal
harem. They may learn while foraging in the company of their
mothers if they succeed in leaving the day roost with them (see
Section 9, Foraging Behavior).
Young males, in contrast, may be ejected early from the
harem, perhaps even before weaning has been completed (see
Section 8, Roosting Behavior). Unless these young males are
able to join a bachelor group quickly and learn to forage with it
(we do not know if males forage in groups) they may be at
greater risk when they leave their natal harem. Alternatively,
juvenile males might remain near the harem roost and forage
with its members even though not roosting with them.
Only occasionally did we capture frail-looking young A.
jamaicensis, but this is not surprising. With a high metabolic
rate and a low protein, high carbohydrate diet one would expect
starvation to be abrupt, perhaps occurring in a single night. In
our bat handling we have observed that the smaller the
frugivore (in terms of age, size, and species) the less tolerant it
is of stress. The small-size species of Artibeus and Vampyressa
may become lethargic and unable to fly, lose control of body
temperature, chill, and die in as little as an hour under stress and
food deprivation. Warming a stressed bat only delays death, but
feeding it a high energy meal, such as a sugar solution, quickly
revives it.
Rain must increase the risk of starvation in young A.
jamaicensis weaned in the rainy season. A series of rainy nights
(perhaps even one) with little or no opportunity for foraging or
reconnoitering for the next night's food source might be lethal
to inexperienced young bats. Wetting greatly increases the
hazard of chilling and loss of temperature control. Stenoder-
matines commonly avoid flying in rain, but might be driven to
do so by hunger. Whereas experienced adults might be able to
forage quickly and effectively during brief intervals when the
rain slackens or stops, the inexperienced bat might not be quite
as efficient. Nightlong rains, particularly a series of them, could
be devastating to whole populations of frugivorous bats,
particularly the young, in a season of fruit scarcity. In
summary, at least three factors might contribute to death by
starvation: nocturnal rains, scarcity of suitable food, and early
ejection of juvenile males from the maternity roost.
PREDATION.?Arboreal snakes are probably the most serious
predators of A. jamaicensis. Roosts in holes in trunks of large
NUMBER 511
25-
20
LU
O 1 5 -
CC
LU
0 .
73
5 -
D - ma|e
= female
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5
AGE IN HALF YEARS
FIGURE 5-8.?Age at last capture of 110 female and 115 male Artibeus jamaicensis marked on BCI and adjacent
mainland as juveniles or subadults and recaptured at least four times. Black bars represent females and white bars
represent males.
trees offer complete protection from snakes unless, as Morrison
observed (see Section 8, Roosting Behavior), vines or saplings
provide access to roosts. Thomas (1974) reported on Boa
constrictor preying on A. jamaicensis in a cave on Isla
Providencia. Handley saw a large snake (probably Spilotes) at
dawn on the roof of Boys' House on BCI, above the entrance of
a Molossus and Myotis roost, with about 18 inches of its head
and body extended beyond the eaves. This was not quite
enough extension to reach the roost entrance under the eaves,
but was probably adequate to catch bats coming into the roost,
especially when the bats made several sorties before actually
entering. Foliage roosts, on the other hand, offer much less
protection from snakes, and most foliage roosters are probably
vulnerable to snake predation. We have seen snakes large
enough to take A. jamaicensis ascend palm fronds, lie almost
invisible along the top side of the stem, and move without
causing visible motion to the frond.
Large opossums (Didelphis marsupialis and Philander
opossum) are efficient bat killers when given the opportunity.
In spite of their formidable teeth, bats in mist nets seem
defenseless against these predators. An opossum crushes the
bat's head with one bite and then consumes the whole bat or all
but the wings. However efficient the opossum may be, it
probably doesn't often have access to bats. Coatimundis
(Nasua narica) might be another predator of bats. We often
have seen coatis in banana plants and in the outermost branches
of fig and breadfruit trees on BCI.
The large carnivorous Vampyrum spectrum eats bats as well
as birds and rodents and might capture A. jamaicensis at
feeding roosts. A captive individual consumed an A. jamaicen-
sis that Handley offered to it. However, V. spectrum seems too
rare on BCI to be much of a mortality factor.
Owls are probably important predators of bats, and bats
milling around a fruit tree might be particularly vulnerable to
74 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
attack. We have attracted the Spectacled Owl (Pulsatrix
perspicillata) to nets by imitating bat squeaks, and have caught
these owls in nets set for bats. Handley watched a Mottled Owl
(Ciccaba virgata) ambushing Myotis nigricans and Molossus
coibensis at their roost at dawn when the bats were milling
about before entering. The owl stationed itself in a tree off to
the side and higher than the roost and made frequent sorties
down through the group of milling bats, usually successfully.
We caught Mottled Owls fairly frequently in nets and
occasionally have caught the Vermiculated Screech-Owl (Otus
guatemalae). At least seven species of owls are known to occur
on BCI, and some of them are rather abundant.
The Bat Falcon (Falco rufigularis), mainly a crepuscular
feeder and known to be an effective predator of bats (Ridgely,
1976), is rare or absent on BCI but nests nearby. The timing of
the departure from and return to day roosts by A. jamaicensis
makes it susceptible to predation by the Bat Falcon. Diurnal
hawks often take bats, especially when they have been
disturbed in their roost during the day. Several African hawks
regularly intercept bats along their flight paths (Black et al.,
1979; Fenton, Cumming, et al., 1977).
Habits characteristic of A. jamaicensis such as lunar phobia
and picking fruit from a tree and carrying it a hundred or more
meters away to be eaten at a feeding roost, are presumably
defensive strategies (Howe, 1979). The frequent use of the
fronds of the spiny-trunked black palm (Astrocaryum standley-
anurri) and the arching fronds of the palm Oenocarpus
panamanus as dining roosts by A. jamaicensis may be a
defensive behavior to protect itself from predators (see Section
8, Roosting Behavior). Response to distress calls of bats that
August (1979) called "mobbing" may also be a defensive
mechanism. At any rate, there are enough seemingly defensive
behavioral traits in A. jamaicensis to suggest that it has
considerable exposure to predators.
ACCIDENTS.?Many netted A. jamaicensis have damaged
wings. Nevertheless, they appear to survive accidents that tear
wing membranes or break fingers. These parts heal remarkably
rapidly and flight is not notably impaired, as we have seen in
our NZP colony. Common sources of injury are fighting among
individuals and encounters with sharp plant spines or thorns.
Bite wounds are most frequent in males, particulary young
males trying to get access to females (observed in the NZP
colony). Judging by netting results, bats may avoid areas in the
forest where spines and thorns are particularly prevalent;
although many, if not most, of the tears in flight membranes
that we have observed must originate from this source. Broken
bones may result from struggles to get free when wings get
tangled. A broken forearm or humerus, rendering the bat
flightless, is invariably fatal.
DISEASE.?Artibeus jamaicensis is known to have been
infected with rabies and trypanosomiasis on the Pacific side of
the Canal de Panama area, but disease in bats is unknown on
BCI.
Summary
On BCI A. jamaicensis made up about 66% of the total
nightly catch of bats year-round. Numbers tended to be highest
when young were first volant and lowest when the population
was composed mostly of subadults and adults.
The entire sample of A. jamaicensis marked between
October 1976 and June 1980, consisted of 8907 bats captured
a total of 15,728 times. Fifty-seven per cent (5061 individuals)
were caught only once, leaving 3846 captured two or more
times. Subsequent captures per bat diminished until we had a
single individual captured 11 times. The probability of
recapturing a bat was roughly the same regardless of the
number of previous captures.
Overall survivorship into the second half year by juvenile A.
jamaicensis was 31%. Survivorship from the second to sixth
half year after marking among bats marked as juveniles was
lower than that of adults and subadults. Dispersal during the
first year is the most likely explanation for this high rate of
disappearance. More frequent recapture of males in the half
year following marking suggests behavioral differences be-
tween the sexes that increase susceptibility to earlier and more
frequent recapture among males.
Juveniles of either sex marked in the first half year are
known to be alive in the second half year in about equal
numbers (30% for males versus 32% for females). But by the
third and fourth half years, the survivorship rate is higher in
females, suggesting that males are more likely to emigrate,
have greater mortality, and possibly learn to avoid nets because
of their higher actual recapture rate during the first year after
mark. Overall, females have higher survival (residency) rates
than males.
Frequency of capture seems to have less to do with age than
with sex. Apparently most bats are easier to capture the first
time, regardless of age: 57% caught once, 25% caught only
twice, 18% caught more than twice, and thereafter the capture
curve levels out
In our sample of almost 17,000 records of A. jamaicensis
(October 1976 to October 1980, adult and subadult females
outnumbered adult and subadult males 55 : 45, while juvenile
females are outnumbered by juvenile males 48 : 52. The
recapture histories of bats marked as juveniles also support the
contention that females have higher survival (or residency)
potential than males.
Among known-age bats, the mean age at last capture was
2.02 years in the females (n = 110) and 1.65 yrs in the males (n
= 115). The average for the entire sample (n = 225) was 1.83
years. The oldest male was four and the oldest female was 6.5
years old. Subsequent to 1980 Handley caught two A.
jamaicensis that were nine years old.
With potentially great longevity, and with most female A.
jamaicensis producing two young each year, the species must
be under severe population controls. Death rate must be high,
but its causes are speculative. Mortality factors include
NUMBER 511 75
starvation, predation, accidents, and disease, but we have little
direct evidence and we have seen few dead bats.
Young of the "spring" birth group are weaned in a season of
abundant food (April-June) at the beginning of the rainy
season. Young of the "summer" group, on the other hand, are
weaned in a season of food scarcity (August-October) in the
middle of the rainy season when they could easily starve before
becoming efficient foragers.
Young A. jamaicensis face a number of risks. With a high
metabolic rate and a low protein, high carbohydrate diet one
would expect starvation to be abrupt, perhaps in a single night
if food sources are not adequate. Young A. jamaicensis and all
ages of the smaller-size species of Artibeus and Vampyressa
become unable to fly, lose control of body temperature, chill,
and die in as little as an hour under stress and food deprivation.
Rain must increase the risk of starvation in young weaned in the
rainy season.
Artibeus jamaicensis relies on a food source that is strongly
pulsed in time and space. It must search out resources for the
future while harvesting a current source. Its behavior and diet
adds risk from predators that may be attracted to the food
source.
Snakes and owls are important predators of bats. Falcons,
opossums, coatimundis, and the large carnivorous bat Vampy-
rum spectrum also are potential predators. There are enough
seemingly defensive behavioral traits in A. jamaicensis to
suggest that it has considerable exposure to predators.
Artibeus jamaicensis is a strong, robust bat that usually
survives accidents that tear the wing membranes or break
fingers. These parts heal remarkably rapidly and flight is not
notably impaired. Many netted A. jamaicensis have damaged
wings. Common sources of injury are fighting among
individuals and encounters with sharp plant spines or thorns.

6. Population Estimates
Egbert G. Leigh, Jr., and Charles O. Handley, Jr.
Between 20 October 1976 and 19 May 1980, Bat Project
participants marked 8907 Artibeus jamaicensis, which had
been captured a total of 15,728 times by 20 October 1980, the
last night of field work covered by this section. Can this record
tell us how long individual A. jamaicensis live, and how many
there are on Barro Colorado Island (BCI)? For purposes of the
ensuing analyses, we will assume that we are sampling the
entire population of A. jamaicensis on BCI, and that it is a
closed population.
A Simple Estimate
AVERAGE LIFETIME.?Suppose A. jamaicensis has an expo-
nential "life table," in which the probability of a bat living past
age y is em y , where e (the base of Napierian logarithms) is
2.71828, and m is the annual death rate per capita. Then, if the
capture effort, averaged over a period during which a quarter of
the bats are replaced, does not vary excessively from one such
period to another, we may estimate the average lifetime 1/m of
these bats by the average time elapsed between first and last
captures of bats captured more than once. We accomplish this
as follows:
1. Let cdt be the probability that a given bat, alive between
time t and time t + dt, is captured during this time interval.
Here, c is the capture rate and dt denotes an "infinitesimal" time
interval. Then the probability of a bat that lives L years being
caught n times in its life is
[(cL)n/n!]exp(-cL)
2. If the probability that a bat's total lifetime lies between L
and L + dL years is (mdL) exp -(mL), then the probability that
a bat will be caught n times in its life is
P(fl) = IT ( m d L ) e x P (-mL)[(cL)n / n!] exp (-cL)
= J r t(cL)n / n!](mdL) exp R r n + c)L]
= (m/c)[c/(c + m)]n+1
Egbert G. Leigh, Jr., Smithsonian Tropical Research Institute, Unit
0948, APO AA 34002-0948, or Apartado Box 2072, Balboa, Republic
of Panama.
Charles O. Handley, Jr., National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560.
3. The average age at which a bat is first captured is
J r (ctdt) exp - (m + c)t
(cdt) exp - (m + c)t
= 1 / (m + c)
4. This time interval l/(m + c) is also the average time
interval between captures, as long as capturing a bat does not
alter its behavior. Thus, the average time between first and last
captures is
[P(2) + 2P(3) + 3P(4) + 4P(5)
(m + c)[P(2) + P(3) = 1/m,
where 1/m is the average lifetime.
The average time elapsed between first and last capture of
bats captured more than once is an exact estimate of average
lifetime, if the life table is exponential. Although the bats we
caught more than once live longer than our records suggest, the
bats we captured more than once tended to be the bats that live
longer than average in the first place, and the errors cancel.
We have calculated the average time between first and last
captures by Bat Project participants of bats first marked by
Morrison (1978b) and Bonaccorso (1979) between 1972 and
1974. Judging from the average interval between first and last
capture by Bat Project personnel of the 33 females and eight
males originally marked by either Morrison or Bonaccorso and
captured more than once during the BCI Bat Project (Table
6-1), the average lifetime of such bats was 1.5 years. If we
consider only females, the estimate of average lifetime is 1.6
years. These bats were two or more years old when first caught
by Bat Project personnel, but if the life table is exponential, the
average expectation of further life does not depend on the initial
age of the bat.
The average time between first and last capture for 301 bats
caught five or more times during the Bat Project is 1.6 years.
This is a surprisingly low figure for bats caught so many times,
because in theory the more times a bat is caught, the greater the
time between first and last capture.
EXPONENTIAL LIFE TABLE.?Our basis for assuming an
exponential life table is as follows. The numbers n(x) of the
77
78 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 6-1.?Interval between first and last capture by the Bat Project of Artibeus jamaicensis first marked on
BCI by Morrison and Bonaccorso.
Category
Both sexes
Females only
0.25*
6
5
0.50
9
6
1.00
2
2
Number of years between first and last capture
1.50
9
8
2.00
4
2
2.50
4
3
3.00
6
6
5.00
1
1
Total
41
33
* Minimum assumed elapsed time for bats caught for the first time and recaptured for the last time in the same half year.
TABLE 6-2.?Observed and expected frequency of capture of Artibeus jamaicensis marked on BCI by Morrison
and Bonaccorso, 1972-1974, and by the Bat Project, 1976-1980.
MORRISON-BONACCORSO BATS
Observed (N = 146)
Expected (69)(0.5274)'1
BAT PROJECT BATS
Observed (N= 15728)
Expected (89O7)(0.4337)"1
69
69
8907
8907
>2
39
36
3846
3863
>3
22
19
1683
1675
>4
11
10
734
727
Number of times caught
>5
3
5
317
315
>6
1
3
146
137
>7
1
1.5
65
59
>8
0.8
21
26
>9
0.4
6
11
>10
0.2
2
5
>11
0.1
1
2
bats marked by Morrison and Bonaccorso and caught at least x
times during the bat project form a geometric series where n(x)
= 69(77/146)*"1 (see Table 6-2). Moreover, one of the most
striking features of the Bat Project's capture records is that the
number n(x) of bats captured at least x times forms a nearly
perfect geometric series: /i(x + 1) = /i(l)A\ where n(l) = 8907
is the total number of bats caught at least once, and A is the
total number of captures of bats caught at least twice, divided
by the total number of captures, or 6821/15728 = 0.4337 (see
Table 6-2).
If the probability that a bat alive at time t is caught between
times t and t + dt is cdt (where capture rate c is constant and dt
is the length of a "short" time interval), then if all bats live the
same lifetime (L), the probability, following the law of Poisson,
that a bat may be caught n times in its life is
[(cL)n/n!]exp(-cL)
On the other hand, if the bats have an exponential life table
with an average lifetime of 1/m, the chance P(x) that a bat will
be captured x times in its life is
P(x) = [m/(c + m)] [c/(c + m)] \
a geometric series in x. This agrees with our observation if
A = c/(c + m).
If these bats have an exponential life table, their age should
not affect their prospects of further life. Is an average lifetime
of 1.6 years reasonable for female A. jamaicensisl Notice that
if the average lifetime 1/m of females is 1.6 years, then m =
1/1.6 = 0.625. Thus, survival rate per year is exp (-m) = 53.5%,
and survival rate per half year is exp (-m/2) = 73.2%.
Half of the females that live long enough to reproduce can
bear a young a half year after they are born (they are products
of the second reproductive episode); all can bear a young every
half year thereafter. If all that can bear a young do so, and if half
the young are female, the expected number of young females a
newborn female bat will bear in her life is
(l/4)(0.732) + (1/2X0.535) [1 + 0.732 + (0.732)2 + . . . ]
= 0.183 + (0.2675)/[I-0.732] x 1.18.
If, as our records show, one of every ten mature female bats
in each breeding season fails to reproduce (see Section 3,
Reproduction in a Captive Colony, and Section 4, Reproduc-
tion on BCI), the population will be very nearly in balance.
Therefore, the average expectation of further life for these bats
probably matches the average lifetime of all female A.
jamaicensis rather closely and suggests that their life table is
indeed exponential.
NUMBER OF BATS.?For the sake of analysis, we shall make
two more assumptions, even though they are not completely
true (see Section 5, Survival and Relative Abundance).
(1) Capturing a bat does not affect the probability of
capturing it again later.
(2) Bats are sampled from a pool in which all individuals
are equally liable to capture.
NUMBER 511 79
Then we may estimate the total number of bats available for
capture during the Bat Project from the number of bats actually
marked, divided by the chance a bat in the pool will be marked,
where the latter is assumed equal to the proportion of marked
bats that are recaptured at least once. In other words, the total
number available during the project equals the number of bats
marked, divided by the chance of marking a bat (equals the
number of bats marked divided by the number of bats
recaptured).
The number of bats available for capture at any one time is
the total number available over the duration of the project,
multiplied by the average bat lifetime 1/m (including both
sexes), and divided by the total duration of the sampling period
(4 years). Another way of saying this is: the total number of
bats available at a given time equals the total available during
the project, times the mean lifetime of a bat, divided by the
duration of the project.
If Artibeus jamaicensis has an exponential life table, and if
all bats "available for capture" are equally likely to be caught,
then the total number of available bats during the four years of
the sampling period is (8907)/(0.4337) = 20535. The number
available at any one time is the total, times the lifetime of these
bats (averaged for both sexes), divided by the four years'
duration of the project, or [(20535)(1.5)]/4 = 7701.
An equivalent way to calculate population size of these bats
is to find the capture rate c by setting A = 0.4337 equal to
c/(c + m), and to assume that the mortality rate m for both sexes
concurrently is 0.667. We find c = 0.5106, which implies that,
on the average, (0.5106)/12 or 4.166% of the bats are caught
each month. As (15,728)/48, or 328, bats were caught per
month, on the average, the total population of A. jamaicensis on
BCI is 328/(0.04166) = 7873.
VALIDITY OF ASSUMPTIONS.?How valid are the assump-
tions behind these calculations? If all available bats are equally
liable to capture and if all bats have equal prospects of further
lifetime, regardless of current age, then the chances of recapture
of all bats marked within a given half year will be the same,
regardless of age or sex.
This is not true. Adults marked in the fall of 1976 and 1977
were at least as likely to be recaptured as the juveniles or
subadults marked at that time, although adults marked later on
were recaptured much less often than were juveniles or
subadults (Table 6-3; and Section 5, Survival and Relative
Abundance, Table 5-9). Few of the adults newly marked in the
fall of 1979 and spring of 1980 were caught again, while
recapture rates were more nearly normal for juveniles and
subadults. Many of these newly marked adults were caught
from peninsulas on the mainland surrounding BCI, where we
netted far less often than on the island. In general, the ratio of
the proportion of newly marked juveniles and subadults, to the
TABLE 6-3.?Percentages, by sex and age class, of Artibeus jamaicensis marked in successive half years on BCI
and subsequently recaptured; proportion of young to adult recaptures; and proportion of adults marked among
total captures of adults (marks and recaptures) caught in each half year.
Age class
Percent recaptured
Juveniles
Subadults
Adults
Ratio of percentage recaptured
Juveniles and Subadults / Adults
Proportion of new marks among captured bats
Number adults marked / Total captures
of adults
Percent recaptured
Juveniles
Subadults
Adults
Ratio of percentage recaptured
Juveniles and Subadults / Adults
Proportion of new marks among captured bats
Number adults marked / Total captures
of adults
Fall
1976
0.3784
0.4185
0.5225
0.7820
1.0000
0.2955
0.3526
0.3841
0.8677
1.0000
Fall
1977
0.3814
0.4413
0.5055
0.8259
0.8044
0.4215
0.4600
0.5050
0.8754
0.7910
Spring
1978
0.7273
0.5404
0.3586
1.6372
0.5380
0.6154
0.5778
0.5364
1.0966
0.4314
Fall
1978
FEMALES
0.3855
0.4879
0.2524
1.8427
0.3787
MALES
0.3093
0.3459
0.3271
1.0151
0.4632
Spring
1979
0.5551
0.5315
0.3668
1.4918
0.5303
0.5368
0.4935
0.2934
1.7762
0.5000
Fall
1979
0.4743
0.3113
0.2194
1.8373
0.2476
0.4220
0.3163
0.2893
1.3404
0.3710
Spring
1980
0.3723
0.2105
0.1237
2.9450
0.3811
0.3109
0.2154
0.2055
1.4383
0.2219
80 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 6-4.?Total captures of Artibeus jamaicensis on BCI in successive half years by sex and age class, by
proportion of young to adult females, by proportion of new marks to total captures (marks and recaptures) among
adult females.
Age class
Juveniles
Subadults
Adults
Juveniles
Subadults
Adults
All bats
Nonadult bats
Juveniles and Subadults / Adult females
Adult female marks / Adult female
captures
Fall
1976
76
251
213
95
201
173
1009
623
2.925
0.836
Fall
1977
247
495
587
285
421
534
2569
1448
2.467
0.624
Total fall nonadults /
Spring
1978
56
241
579
48
232
522
1678
577
0.997
0.496
Fall
1978
FEMALES
85
354
296
MALES
101
200
256
TOTALS
1292
740
Spring
1979
307
197
771
308
232
514
2329
1044
PROPORTIONS
2.500
0.348
Total fall adult females = ?306 ~
1.354
0.477
2.950
Fall
1979
397
535
666
506
409
658
3171
1847
2.773
0.233
Spring
1980
401
49
533
367
132
318
1800
949
1.781
0.364
Fall
1980
612
543
544
625
364
430
3118
2144
3.941
0.248
proportion of newly marked adults recaptured subsequently,
was higher the greater the proportion of adults already marked
(Table 6-3).
Our assumption that all available bats are equally liable to
recapture is clearly wrong. It seems, rather, that as more bats
were netted, we reached a point where most of the adult bats on
BCI had been marked, so most bats available for marking on
the island were juveniles and subadults. Thereafter, many of the
bats marked as adults resided in localities where prospects of
recapture were not great or they learned to avoid the nets.
Not only are bats in certain places more liable to recapture,
younger bats are more liable to recapture than older ones. The
ratio of the total number of juveniles and subadults of both
sexes to the number of adult females handled (counting each
instance of capture) in the fall of 1976 was 2.925; combining all
the fall catches of the sampling period together, it was 2.950
(Table 6-4). Because adult females can have no more than two
young a year, adult females must be nearly twice as hard to
catch as juveniles of either sex.
A Refined Estimate
Population size in these bats can be better estimated after two
intermediate steps.
(1) Calculating mortality rates for both sexes.
(2) Calculating the total numbers of marked bats of each
sex alive in successive half years (Dowdeswell et al.,
1940; Fisher and Ford, 1947).
The first step enables the second, because the total number of
individuals M(t) alive in half-year t of the Bat Project that were
marked earlier is the number m'{\) marked in the first half year
(fall 1976), times the proportion p(t- 1) surviving to half-year
t, plus the number m'(2) marked in the second half year (spring
1977) times the proportion p(t-2) of those surviving to
half-year t, and so on. In summary:
M(t) = m'(l)p(t- 1) + m'(2)p(t-2) + . . . + m'( t - l)p(l).
MORTALITY ESTIMATES.?If we assume that the numbers of
A. jamaicensis on BCI do not change substantially from year to
year, the simplest way to calculate the mortality of adults is to
consider the recaptures of a sample of marked bats as long after
they were first marked as possible. The bats marked by
Morrison (1978b) and Bonaccorso (1979) provide a suitable
sample. Between 1972 and 1974 they marked 1212 A.
jamaicensis, of which about half were female. Of these females,
47 were caught by the Bat Project after 1 July 1977. Because 93
of the 178 adult female A. jamaicensis marked by the Bat
Project in the fall of 1976 were recaptured after 1 July 1977, it
seems reasonable to assume that 93/178 of the females marked
by Morrison and Bonaccorso, and still living in the fall of 1976,
were recaptured after 1 July 1977. If so, then 47(178/93), or 90,
of Morrison and Bonaccorso's female bats were alive in the fall
of 1976, implying a survival rate of (90/606)1/35, or 58%, a
year, and an expectation of further life of 1.835 years.
Similarly, 16 of their marked male bats were caught after 1 July
1977. As 58 of 151 adult males marked by the Bat Project in the
NUMBER 511 81
fall of 1976 were caught after 1 July 1977, roughly 16(151/58),
or 42, of the bats marked by Morrison and Bonaccorso were
alive during the fall of 1976, implying a survival rate of 46.7%
a year. If the population were declining, these estimates would
be too high, and vice versa.
A second way to calculate survival rate is to consider the
dates of first capture of the bats recaptured in a given half year.
Let n(t, x) be the number of bats captured in half-year t that
were first marked in half-year x, and let m'(x) be the total
number of bats marked in half-year x (Tables 6-5 and 6-6).
Then m'(x)p(t-x) is the total number of bats marked in
half-year x surviving to half-year t. If a fraction c(t) of the bats
alive in half-year t are captured then, n(t, x) = c(t)m'(x)p(t - x).
If the bats have an exponential life table, then
p ( t - x ) = exp[-m(t-x)/2] ,
where exp (-m) is the average survival rate per year. Moreover,
n(U = c(t) exp [-m(t -
suggesting that we calculate m as the coefficient of regression
of log [n(t, x)/m'(x)] on x.
This method of estimating m suffers from the disadvantage
that bats marked later in the project are more likely to be from
infrequently sampled sites. Thus, bats first marked in half-year
7 are less likely to be recaptured in half-year 8 than already
marked bats caught in half-year 7. On the other hand, this
estimate of m does not depend on the stability of the bat
population as a whole.
Nonetheless, estimates (Table 6-7) of survival rates of
female bats based on recaptures for half-year 7 and half-year 9,
for which the correlation between the half-year x of marking
and the logarithm of the proportion n(t, x)/m'(x) of bats marked
then that were recaptured in half-year t is relatively close, agree
with each other, and with the estimate based on bats marked by
Morrison and Bonaccorso and recaptured by the Bat Project.
The average of the former two estimates is 57.4%, compared
with 57.99% from the Morrison and Bonaccorso bats.
On the other hand, estimates of survival rates of male bats
based on recaptures for half-years 7 and 9 average 37.2% a
year, markedly lower than the 46.7% estimated from recaptures
of male bats marked by Morrison and Bonaccorso. Do older
males survive better? The 46.7% figure is based on a rather
small sample of recaptures. Another piece of evidence is the
recapture in the fall of 1981 of a male marked by Morrison and
Bonaccorso. If 37.2% of the males survive each year, a male
has one chance in 4000 of surviving the 8.5 years to the fall of
1981, so the chances are 1 in 7 that one of their 606 bats would
still be living, and perhaps half that, had it been alive, we would
have caught it then. That capture record suggests, but does not
prove, that at least some older males survive rather better.
Finally, if the population is stable, we may calculate adult
mortality rates from the proportions n(x, t)/[m'(x) + n(x)] of
bats marked in a given half-year t among the total number of
bats?both marks, m\x), plus recaptures, n(x)?caught in later
half years. If m'(x) + n(x) = c(x)N(x), where c(x) is the
proportion of the N(x) bats alive in half-year x that were caught
during that half year, while
n(x, t) = c(x)m'(t) exp -m(x -1)/2,
then n(x, t)/[m'(x) + n(x)] = [m'(t)/N(x)] exp -m(x -1)/2. If N
is constant, the regression on x of the logarithm of this
proportion is m/2. If the bat population is growing by a factor
exp (r/2) per half year, then N(x) = N(t) exp r(x -1)/2, and our
regression gives (m + r)/2.
Mortality estimates for bats, both male and female, marked
in the fall of 1976 and the spring of 1978, agree with each other,
and are only slightly lower than those calculated from marking
dates of bats recaptured in the fall of 1979 and the fall of 1980.
Mortality estimates for bats marked in the fall of 1977 are much
lower, but like those for bats marked in the spring of 1978, the
fall 1977 estimates are based on strong correlations, illustrating
the uncertainties in our calculations.
If the chances of capturing a bat depend on its age class, then
this estimate requires that the age composition of bats captured
in successive half years be the same. If the chances of capturing
a bat depend on whether it is already marked, then the
proportion of recaptures among the bats handled should also be
constant. Finally, if chances of recapture vary from place to
place, netting effort should be distributed over the island in the
same way during successive half years.
Are our figures true mortalities? Although bats do occasion-
ally move between BCI and the surrounding mainland, this
exchange does not seem to be great (see Section 7, Move-
ments). We do not think we are mistaking emigration for
mortality. However, some bats do lose their necklaces. Adding
together the intervals between time of first necklacing and of
last recapture for each bat concerned, our project has monitored
bats carrying Morrison and Bonaccorso wing bands for over
fifty bat years. During this interval, five bats lost their
necklaces, suggesting that the survival rate of necklaces is 90%
a year. If so, the average survival rate of A. jamaicensis is 11 %
higher than our regressions suggest, perhaps between 62% and
65% a year for adult females.
Given the survival rate of juveniles relative to adults, and the
breeding rate of adult females, the survival rate of adult females
must be near 60% a year if the population is to be in balance. To
show this, we make the following assumptions and observa-
tions. Half of the females (those that are born in the second
reproductive episode) can bear a young a half year after birth;
all can bear a young when they are a year old, and all can breed
once each half year thereafter; half their offspring are female.
Twenty-eight of the 74 juvenile females caught in the fall of
1976 were recaptured in successive half years, while 87 of the
178 adult females marked then were recaptured later (see
Section 5, Survival and Relative Abundance, Table 5-9). Thus,
a marked juvenile female had 0.7242 times the chance of being
recaptured as an adult as did an adult female marked then. If in
general, the chance of a juvenile female surviving through its
82 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 6-5.?Numbers of female Arlibeus jamaicensis marked on BCI in successive half years by age class, by
numbers n(x, y) of these recaptured in later half-years y, and by number n(x) of recaptures in half-years x of these
bats marked in previous half years; and based on these values, proportions n(t, x)/m'(x) of these bats recaptured
in selected half-years t among those marked in earlier half-years x, and proportions n(x, t)/[m'(x) + n(x)] of bats
marked in selected half years among those caught in later half years.
Females
Marked
Juveniles
Subadults
Adults
Total [m'(x)]
Recaptures from half-year y
1
3
4
5
6
7
8
Total
Recaptured/Marked
n(9, x)/m'(x)
?(8, x)/m'(x)
?(7, x)/m'(x)
n(x, l)/[m'(x) + n(x)]
?(x. 3)/Im'(x) + n(x)]
n(x, 4)/Im'(x) + ?(x)]
1
Fall
1976
74
227
178
479
16/479
23/479
33/479
3
Fall
1977
236
358
366
960
91
91
41/960
47/960
88/960
91/1051
4
Spring
1978
66
198
290
554
Recaptures n(x,
68
181
249
38/554
31/554
67/554
68/803
181/803
5
Fall
1978
83
289
103
475
Half-year x
6
Spring
1979
272
141
368
781
7
Fall
1979
331
257
155
743
8
Spring
1980
368
19
194
583
y) in half-year x of bats first caught in half-year y
27
81
61
169
46/475
32/475
100/475
27/644
81/644
61/644
36
102
74
114
326
Proportions
76/781
75/781
183/781
36/1107
102/1107
74/1107
33
88
67
100
183
471
115/743
107/743
33/1214
88/1214
62/1214
23
47
31
32
75
107
315
157/583
23/898
47/898
21/898
9
Fall
1980
500
286
135
921
16
41
38
46
76
115
157
489
16/1410
41/1410
38/1410
first year is 0.7242 times the chance (p2) of an adult female
surviving a full year, and if a female has a 1/4 chance of bearing
a female young when it is a year old, and a 1/2 chance of doing
so each half year thereafter, then the number (Ro) of female
young a newborn female A. jamaicensis can expect to bear
during her life is
Ro = 0.7242
= 0.1810p + 0.362/^/(1 - p ) .
If survival rate p2 per year is 0.5625 (so p = 0.75), then
Ro = 0.95; if p2 = 0.6 (sop = 0.7746), then Ro = 1.10; and
ifp2 = 0.64 (sop = 0.8), then Ro = 1.30.
In fact, not all females breed in each breeding season. In six
reproductive episodes in our captive colony wild-caught adult
females were pregnant in 66 of 72 chances (91.7%), multipa-
rous captive-born females were pregnant in 12 of 14 chances
(85.7%), and primiparous captive-bom females were pregnant
in 14 of 20 chances (70%) (see Section 3, Reproduction in a
Captive Colony, Tables 3-4 and 3-5). On BCI in the month of
April, when all females should be reproductive, we invariably
caught a few nonreproductive adult females and some
subadults who failed to reproduce on time (undoubtedly
9-month-old young of the previous July-August birth-group).
For example, in April 1978,9 of 102 adult females caught were
nonreproductive, and we caught 22 subadult females; in April
1979, 7 of 47 newly marked adult females were nonreproduc-
tive. We can make a minimum correction for this by
multiplying our values of Ro for different survival rates by 0.89,
the percentage (133/149) of adult females caught in 1978 and
NUMBER 511 83
TABLE 6-6.?Numbers of male Artibeus jamaicensis marked on BCI in successive half years by age class, by
numbers n(x, y) of these recaptured in later half-years y, and by number n(x) of recaptures in half-years x of these
bats marked in previous half years; and based on these values, proportions ?(t, x)/m'(x) of these bats recaptured
in selected half-years t among those marked in earlier half-years x, and proportions ?(x, t)/[m'(x) + n(x)] of bats
marked in selected half years among those caught in later half years.
Males
Marked
Juveniles
Subadults
Adults
Total [m'(x)]
Recaptures from half-year y
1
3
4
5
6
7
8
Total
Recaptured/Marked
?(9, x)/m'(x)
?(8, x)/m'(x)
n(7, x)/m'(x)
?(x. l)/[m'(x)+n(x)]
n(x,3)/[m'(x)+?(x)]
fl(x,4)/[m'(x)+n(x)]
1
Fall
1976
88
173
151
412
3/412
9/412
9/412
3
Fall
1977
261
300
299
860
79
79
10/860
18/860
56/860
79/939
4
Spring
1978
52
135
220
407
5
Fall
1978
97
159
107
363
Half-year x
6
Spring
1979
272
154
242
668
7
Fall
1979
410
196
197
803
8
Spring
1980
341
65
73
479
Recaptures ?(x, y) in half-year x of bats first caught in half-year y
55
235
290
13/407
22/407
44/407
55/697
235/697
14
50
60
124
15/363
31/363
61/363
14/487
50/487
60/487
19
65
57
101
242
Proportions
46/668
50/668
164/668
19/910
65/910
57/910
9
56
44
61
164
334
90/803
126/803
9/1137
56/1137
44/1137
9
18
22
31
50
126
256
114/479
9/735
18/735
22/735
9
Fall
1980
496
198
101
795
3
10
13
15
46
90
114
291
3/1086
10/1086
13/1086
1979 that were actually breeding.
There may be other errors in our calculations. On the one
hand, spring-born juveniles should survive better than fall ones;
on the other, our figures for juvenile mortality do not include
deaths before the juveniles are old enough to fly into our nets.
All in all, we believe the survival rate of adult female Artibeus
jamaicensis is between 60% and 64% a year.
ESTIMATE OF SURVIVING MARKED BATS IN SUCCESSIVE
HALF YEARS.?Let M ^ t ) represent the number of marked
adult female bats alive at the beginning of half-year t, and
Mrf(t) be the number of marked subadult female bats also
alive then. In addition, p represents the survival rate of adult
females per half year.
Eighty-three of the 227 subadult bats marked in the fall of
1976 were recaptured in succeeding half years, while 87 of 178
adults marked then were recaptured later (Section 5, Survival
and Relative Abundance, Table 5-9), suggesting that a subadult
female was 0.8010 times as likely as an adult to survive her
next half year. If this is true in any half year, then a juvenile
female is (0.7242)/(0.8010) = 0.9041 times as likely as an adult
female to survive her next half year. If we make the convention
that a fraction -ip of the adults, a fraction 0.8010 Jp of the
subadults, and a fraction 0.9041 <p of the juveniles marked in
a given half year survive to the beginning of the next half year,
and that juveniles become subadults, and subadults become
adults, at that time, then we may assume the number Msf (t) of
marked subadult females at the beginning of a half year to be
0.9041 <p m^ (t - 1), where mjf (t - 1) is the number of juvenile
females marked in half-year t - 1.
The marked adult females alive at the beginning of half-year
84 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 6-7.?Estimates of mortality rate (m) and survival rate e"" per year of Artibeus jamaicensis marked on BCI
and recaptured in several half years.
Regression on x of
log n(9, x)/m'(x)
log n(8, x)/m'(x)
log n(7, x)/m'(x)
log[m'(x) + ?(x)]/n(x, 1)
log [m'(x) + n(x)]/n(x, 3)
log [m'(x) + n(x)]/n(x, 4)
Regression on x of
log n(9, x)/m'(x)
log n(8, x)/m'(x)
log ?(7, x)/m'(x)
log[m'(x) + ?(x)]//t(x,l)
log [m'(x) + ?(x)]/n(x, 3)
iog[m'(x)+?(x)]/n(x,4)
(1/2)m
0.2911
0.1814
0.2647
0.3178
0.3746
0.3175
0.5019
0.3417
0.4876
0.5452
0.6416
0.5401
Coefficient of regression
1/m
FEMALES
1.718
2.756
1.889
1.573
1.335
1.575
MALES
0.996
1.463
1.025
0.917
0.779
0.926
e m
0.559
0.696
0.589
0.530
0.437
0.530
0.367
0.505
0.377
0.336
0.277
0.340
r2
0.9492
0.8154
0.9338
0.9274
0.9781
0.9869
0.9746
0.8590
0.9944
0.9150
0.9669
0.9701
t include
(1) <p m ^ t - 1) adult females marked the preceding half
year (assumed marked in the middle thereof, so that
they have had half a half year in which to die, so a
fraction Jp have survived to the beginning of half-year
0,
(2) 0.8010 <p m j t - l ) subadult females marked in
half-year t - 1,
(3) a proportion p of the Mrf(t - 1), marked adults alive at
the beginning of half-year t - 1, and
(4) 0.8010 pMrf(t - 1) adults, which already were marked
and subadult at the beginning of half-year t - 1.
To summarize:
Mff(t) = 0.9041 V p m ^ t - l )
MtfCt) = p[0.8010Mrf(t- 1) + MrfCt- 1)]
+ Vp[0.8010mrf(t-l) + m r f ( t - l ) ] .
If p = 0.1 All, so that the survival rate of adult females, with
their necklaces, is p2 = 55.9% a year, then the maximum
number of marked adult females was 1534 on 1 July 1980.
If we conclude from Table 5-9 (Section 5, Survival and
Relative Abundance) that juvenile males marked in half-year t
have probability 0.7693 q1/2 of surviving to the beginning of
half-year t + 2, while subadult males alive at the beginning of
half-year t + 1 have probability 0.9180 q of living another half
year, where q is the survival rate of adult males per half year,
then the number of marked subadult males alive at the
beginning of half-year t is
lAJfy = 0.8380 ^ m j m ( t - l )
and the number of marked adult males alive at the beginning of
half-year t is
M . J 0 = rtO.918OM.Jt-l) + M . J t - 1 ) ]
+ <q [ 0 . 9 1 8 0 m j t - l ) + m . J t - 1 ) ] .
If q = 0.6058, so that survival rate of marked males with their
necklaces is q2 = 36.7% a year, then the maximum number of
marked adult males was 829 on 1 January 1980.
How do our estimates compare with calculations for other
species? Most available data are for temperate-zone species.
Rice (1957) proposed an annual survival rate of 46% for Myotis
austroriparius in Florida, the rate necessary to maintain a
balanced population given his calculated birth rate for the
population. Davis et al. (1962) assumed a constant mortality
rate for Tadarida brasiliensis after the initiation of flight and
estimated an adult survival rate of 70%-80% with a maximum
age of 15 years. Stebbings (1966) calculated a survival rate of
75% and a life expectancy of four years for two species of
Plecotus in England. Similarly, Dwyer (1966) suggested 75%
for Miniopterus schreibersii in Australia.
Mean annual survival rates for 20 temperate zone species
ranged mainly from 40% to 80%, but extremes of 4% and 98%
were also reported (Tuttle and Stevenson, 1982). All of these
were based on banding studies of individuals of unknown ages.
Studies based on known-age cohorts are available mainly for
summer roosts of temperate-zone animals, and estimates of
survivorship are similarly variable. A summary of the results
and some discussion of the problems inherent in such studies
were presented by Tuttle and Stevenson (1982).
Fleming (1988) used three separate sets of data to analyze
NUMBER 511 85
survivorship in Carollia perspicillata in Costa Rica. Based on
recapture data, he concluded that relatively few individuals
remain in the population after five years, but his was an open
population, with no way of separating dispersal from mortality.
Young females disappeared at a higher rate than young males,
a difference he attributed to dispersal rather than mortality. He
found no differences in survivorship of young born at different
times of the year (different birth groups). Adult males and
females had similar survivorship rates (around 60%).
Annual survivorship estimates based on census data for a
single cave population of C. perspicillata ranged from 40% to
82% (Fleming, 1988). Again, the data are confounded with the
problem of dispersal, and his estimates based on survival across
two years yielded estimates of 57% for males and 43% for
females. A survivorship curve based on toothwear data yielded
values within the ranges of the estimates based on the other
methods (Fleming, 1988).
ESTIMATING POPULATION SIZE.?The number of adult bats
actually marked provides minimum estimates of the number of
adult bats in the population from which we were netting. Tables
6-8 and 6-9 suggest that there were at least 1500 adult females
and 800 adult males in the population between 1 January 1980
and 1 January 1981.
Another minimum estimate of the number of adult female
bats is the number required to produce the numbers of juvenile
and subadult bats marked in a given year. In 1980, we marked
1173 female and 1100 male juvenile and subadult bats (Table
6-8). If a female produces 1.78 young a year (corresponding to
the 89% pregnancy rate of adult females netted in April 1978
and April 1979), it would take about 1300 adult females to
produce this many young.
Another seemingly more accurate way to estimate the
number of adult females is to divide the number of adult
females marked before half-year t and presumed to be alive in
the middle of that half year, 0.8802 M^(t), by the proportion of
adult females caught that half year that were marked in
previous half years. Averaging such estimates for those half
years when fewer than half the adult females caught were
unmarked, we were netting from a population of about 1800
adult females. Similarly, we were netting from a pool of about
850 adult males.
If we assume that, averaging from year's end to year's end,
there are roughly as many nonadult bats as adult females, then
our minimum estimates suggest we were netting from a pool of
TABLE 6-}
New marks
Juveniles m^t )
Subadults m^ t )
Adults m ^ t )
Recaptures*, nfi)
At beginning of half yearf.t
Total marked adults M^ t )
Total marked subadults M^t)
New marks
Juveniles nijm(t)
Subadults mim(t)
Adults m ^ t )
Recaptures*, ?m(t)
At beginning of half year*. ?
Total marked adults M J t )
Total marked subadults Mm(t)
i.?Number of Artibeus jamaicensis marked on BCI alive in successive half yean.
1
Fall
1976
74
227
178
88
173
151
3
Fall
1977
236
358
366
91
282
261
300
299
79
178
4
Spring
1978
66
198
290
249
793
188
52
135
220
290
555
170
5
Fall
1978
83
289
103
169
1126
53
97
159
107
124
698
34
Half-year t
6
Spring
1979
FEMALES
272
141
368
326
1200
66
MALES
272
154
242
242
639
63
7
Fall
1979
331
257
155
471
1394
216
410
196
197
334
721
177
8
Spring
1980
368
19
194
315
1532
263
341
65
73
256
829
267
9
Fall
1980
500
286
135
489
1534
293
496
198
101
291
754
222
10
1480
398
800
326
* Each bat recaptured in a given half year is counted once, regardless of how often it was caught in that half year.
t Total number M^t) of marked adult females at beginning of half-yeart is [M^t -1) 0.801 + M ^ t -1)] 0.7747 + [m^t -1) 0.801 + m ^ t -1)] 0.8802.
% Total number M^(t) of marked subadult females at beginning of half-year t is (0.9041)(0.8802) m^t -1), where (0.8802)2 = 0.7747.
* Total number Mm( t) of marked adult males at beginning of half-year t is [0.918 Mm( t -1) + M J l -1)] 0.6058 + [0.918 m . J t -1) + m ^ t -1)] (0.6058).
* Total number M ra(t) of marked subadult males at beginning of half-year t is (0.8380)(0.7783) m>n(t -1), where (0.7783)2 = 0.6058.
86 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 6-9.?Number of Arlibeus jamaicensis marked on BCI: number of non-adult bats marked, number of
adults already marked at beginning of half year, proportion of these marked bats recaptured, proportion of adult
bats caught that had been recaptured in previous half years, and estimated number of adults in successive half
years.
Number marked that half year
Total marked, m^t)
Nonadults marked, rr^(t) - m^(t)
Adults already marked, M^(t)
Proportion of marked bats recaptured that half year.
P. (t) = nf (t)/IM^(t) + Mrf(t)]
Proportion of adults previously recaptured,
Qf (0 = ?f ( 0 / K W + mrf(t)]
Ratio of number marked to efficiency of recapture,
m^tyiOOOP^t)
Estimated population size,
VpMrfW/QfC)
Number marked that half year
Total marked, mm(t)
Nonadults marked, mm(t) ? m^Ct)
Adults already marked, M^ft)
Proportion of marked bats recaptured that half year,
Pm(t) = nm(ty [ M ^ t ) + Mm(t)]
Proportion of adults previously recaptured,
Qm(0 = ?m(0/l?m(t) + m j l ) ]
Ratio of number marked to efficiency of recapture,
mm(t)/1000Pm(t)
Estimated population size,
VqMm(t)/Qm(t)
3
960
594
282
0.323
0.199
2.97
1247
860
561
178
0.444
0.209
1.92
663
4
554
264
793
0.254
0.462
2.14
1511
407
187
555
0.400
0.569
1.02
759
5
475
372
1126
0.143
0.621
3.32
1596
363
256
698
0.172
0.537
2.11
1012
Half-year t
6
FEMALES
781
413
1200
0.258
0.470
3.03
2247
MALES
668
426
639
0.345
0.500
1.94
995
7
743
588
1394
0.293
0.752
2.19
1632
803
606
721
0.372
0.629
2.16
892
8
591
387
1532
0.175
0.619
3.38
2178
479
406
829
0.234
0.778
2.05
829
9
921
786
1534
0.268
0.784
3.44
1722
795
694
754
0.298
0.742
2.67
791
3800 bats (1500 adult females, 800 adult males, and 1500
juveniles and subadults), whereas the latter method suggests
4450 (1800 adult females, 850 adult males, and 1800 juveniles
and subadults).
These estimates are riddled with assumptions, of which the
most conspicuous are (1) marking does not affect an adult's
prospects of subsequent capture, and (2) all adults are equally
liable to capture. The first assumption is not very plausible,
although it is admittedly difficult to distinguish between the
greater difficulty of catching older bats, which is obvious from
our data, and the greater difficulty of catching marked bats. If
capture effort were spread evenly enough to assure that all live
bats of a given age were equally liable to capture, one might
expect the ratio of the number of bats marked, or at least of the
number of nonadult bats marked, to the proportion of marked
bats recaptured, to be constant, or nearly so. It is not (Table
6-9). Despite these problems, these estimates are close enough
to the minimum estimates that further refinement of our counts
of adult bats seems unnecessary.
RELATIONSHIP OF POPULATION SIZE AND DISTRIBUTION.?
The Bat Project apparently was netting from a pool of about
4000 A. jamaicensis. How big an area did this population
represent? To find out, we calculated the number of bats alive
on 1 July 1979 that were marked at various points on the
mainland, and asked how many of these were recaptured in the
fall of 1979 and where they were caught. Tables 6-10 and 6-11
show that, although there is some exchange of bats between
BCI and nearby mainland sites, bats from these areas do not
form a common pool.
The average maximum distance between recaptures of A.
jamaicensis captured three or more times is about 1.5 km (see
Section 7, Movements). As BCI is roughly a rectangle 3 km by
5 km, and as half the perimeter of the island is surrounded by
nearby mainland approximately a kilometer distant, we shall
assume that our 4000 bats represent a land area of 3.5 km by 5.5
km, or roughly 20 km2, implying 200 bats per square kilometer.
We accordingly conclude that BCI supports an average of 3000
A. jamaicensis.
NUMBER 511 87
TABLE 6-10.?Exchange of Artibeus jamaicensis between BCI and the mainland.
Locality of
first marking
Bohio Peninsula
Mona Grita Point
Old Frijoles Road
Barro Colorado Island
Number* of
marked bats
still alive
1 July 1979
136
17
107
1855
BCI
2
1
1
675
Number of marked bats
recaptured fall 1979
Bohio Peninsula
2
0
0
2
* Number calculated assuming a survival rate of 50% a year. If there are two marked females for every marked
male, as is true for the population at large, then the annual survival rate is 2/3 (0.56) + 1h (0.37) = 0.50.
TABLE 6-11.?Proportion of recaptures to marks among Artibeus jamaicensis netted on the mainland near BCI.
Number marked
Number recaptured
from Standley 21
from elsewhere on BCI
first marked at Bohio
in January 1978
in December 1978
Jan
1978
114
8
9
0
0
Bohio
Dec
1978
67
1
1
7
0
Apr
1979
105
12
13
4
9
Jan
1979
33
0
3
0
0
Frijoles
Apr
1979
151
0
4
0
0
Summary
During the five years of field work covered by this volume,
we marked 8,907 individual Artibeus jamaicensis and captured
them a total of 15,728 times. Data on multiple captures form a
nearly perfect geometric series, suggesting an exponential life
table. Assuming an exponential life table, the average lifespan
of these bats is 1.6 years, based on the average time between
first and last capture of individuals captured more than once. If
average lifespan is 1.6 years, and if adult females bear a young
in each breeding season, the average female will produce 1.18
young in her lifetime. Our records indicate that one of every ten
females fails to reproduce in each reproductive season, a figure
that yields a population that is nearly in balance.
Survival rates based on bats marked between 1972 and 1974
and recaptured during 1976-1980 were 58% for females and
46.7% for males, if the population was stable during this
period. Similar rates calculated for bats recaptured during a
given half year, independent of the stability of the population as
a whole, are similar for females (57.4%), but different for males
(37.2%). One possible explanation for this difference is that
older males survive better. Our data on necklace loss, coupled
with reproductive data suggest that the actual survival rates are
somewhat higher, perhaps on the order of 60%-64% for
females.
Population estimates based on mark-recapture methodology
and on capture rate are surprisingly close, at 7701 and 7873, but
both are flawed by assumptions of equal probability of capture
that clearly are not valid. More refined estimates of surviving
marked bats in successive half years suggest that there were a
maximum of 1,534 marked females and 829 marked males in
1980. In that year we marked 2,273 juvenile and subadult bats,
suggesting a minimum of 1,300 adult females to produce that
many young. Mark-recapture methodology for successive half
years yields estimates of 1,800 adult females and 850 adult
males. If we assume there are roughly as many nonadults as
adult females during a year's time, then the minimum estimates
suggest 3,800 bats and the higher ones about 4,500.
Assuming a pool of 4,000 bats taken from a land area of
about 20 square kilometers that includes BCI and parts of the
surrounding mainland, we estimate there are about 200 A.
jamaicensis per square kilometer, or a population of about
3,000 on the island itself.

7. Movements
Charles O. Handley, Jr., Alfred L. Gardner,
and Don E. Wilson
With our abundant capture and recapture data we hoped to
trace the movements of Artibeus jamaicensis on Barro
Colorado Island (BCI) and to estimate the extent of these
movements around each capture locality. However, conven-
tional mark and recapture analyses are not as productive for
bats as they are for some other organisms, partly because bats
are comparatively less frequently recaptured. The recapture rate
for our 8907 A. jamaicensis averaged 1.8 per bat Less than
50% (3846) were recaptured at all, and less than 20% (1683)
were captured three or more times (see Section 5, Survival and
Relative Abundance, Table 5-2). Therefore, only a few
individuals were useful in describing distributions and patterns
of movements.
A mark at one locality and recapture elsewhere does not
reveal the focal "home base" or roost locality. Roosts are
difficult to locate except by radio tracking, which we did not
routinely do. Except for maternity roosts in caves, tree holes,
and man-made structures, the "home base" is likely to be
temporary anyway. Artibeus jamaicensis frequently traveled
long distances (up to about 6 km) between capture sites on BCI
and mainland. The distance from the center of BCI to any point
on its perimeter is only about 3 km, and the maximum distance
between points on the perimeter is about 5 km. Therefore, the
potential home range of an A. jamaicensis on BCI includes the
entire island and perhaps parts of the adjacent mainland as well.
It proved fruitless to distinguish between mark and recapture
records and between mark and recapture localities on an
individual basis when describing distributions. Therefore, we
pooled all records for analysis rather than treating only the
records of individual bats. This greatly increased the sample
size for each capture locality and reduced some kinds of biases
such as that caused by unusually long movements. We
converted these records to percentages of the total for a
particular locality so as to examine movements for that site. We
Charles O. Handley, Jr., and Don E. Wilson, National Museum of
Natural History, Smithsonian Institution, Washington, D.C. 20560.
Alfred L. Gardner, NERC, U.S. Fish and Wildlife Service, National
Museum of Natural History, Washington, D.C. 20560.
then tested and manipulated our data to explore effective means
of describing home ranges and movement patterns.
Measures of Movements and Capture Effort
We tabulated captures by species and by half years on a
matrix of locality groups, totalled the number of A. jamaicensis
captures recorded at each locality group, and summarized the
entire marking interval (October 1976 through October 1980;
Figure 7-1, Table 7-1). We then analyzed the records of all
individuals recorded from a locality that were caught again in
the same half year at that and other localities. These we called
"other-captures" (tabulated by the column number of the
locality of subsequent capture along the horizontal axis of
Table 7-1). For example, other-captures at Lutz (642) of the
5309 Lutz records for A. jamaicensis, are under column 1 and
other-captures of Lutz bats at Shannon-AMNH (107) are in line
1, column 3.
We found that the proportion of other-captures to the total
number of captures from any given locality was extremely
variable (from 1% to 43%; Figure 7-2 and Table 7-2).
Contributing to this variation were factors such as the
proximity of netting sites to other netting locations, and the
frequency of netting (netting effort) at each locality.
We also found that the proportion of other-captures to total
captures was not always dependent on netting effort For
instance, although both sites had similar netting effort,
Shannon-AMNH (730 records of A. jamaicensis) and Bohio
(746 records) had 42% and 17% other-captures (Table 7-2),
respectively. Barbour-Hood (640 bats) and Standley End (649),
also with similar netting effort, had 36% and 22% other-
captures, respectively. In contrast, at Chapman with 29% and
Lutz with 30% other-captures, total A. jamaicensis numbered
388 and 5309, respectively.
The localities that had from 36% to 43% other-captures are
centrally located on BCI (Figure 7-2, Table 7-2). Localities
with 17% to 35% other-captures (excepting Barbour Stream
with 24% and Lutz with 30%) are all marginal locations near
the lakeshore. The lowest other-capture percentages are 17% at
Drayton End and the isolated mainland localities (Bohio, 17%;
89
90 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
4 5 46 47 48 49 50
11ii1
0 1 2 3 4 5
kilometers
FIGURE 7-1.?Distribution of locality groups (aggregations of localities) where bats were captured on BCI and
adjacent mainland (from Table 7-1). The locality groups are as follows: (1) Lutz; (2) Barbour-Hood; (3)
Shannon-AMNH; (4) Shannon-Balboa; (5) Lake-Wheeler; (6) Barbour Stream; (7) Miller Ridge; (8) Fuertes; (9)
Conrad; (10) Plateau; (11) Drayton End; (12) Armour End; (13) Zetek 21; (14) StandQey Ridge; (15) Standley
End; (16) Orchid Island; (17) Gross Point; (18) Chapman; (19) Harvard; (20) Mona Grita; (21) Gigante; (22)
Frijoles Rd.; (23) Bohio; (24) Buena Vistt; (25) Pena Blanca.
NUMBER 511 91
4 6
4 5
I ? ?? ? ! . . . . I
2 3
kilometers
FIGURE 7-2.?Percentage of other-captures in the total records (total individuals plus other-captures of them) in
capture suites of Artibeus jamaicensis at locality groups on BCI and the adjacent mainland, 1976-1980. Data are
from Table 7-2. Isolines arbitrarily enclose locality groups with similar percentages of other-captures. Marginal
numbers identify kilometer squares (see Appendix, Methods of Capturing and Marking Tropical Bats).
92 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
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NUMBER 511 93
TABLE 7-2.?Tabulation of total records, total other-captures, and percentage of other-captures (see text for
explanation) of the total number of Artibeus jamaicensis in each locality group on BCI and adjacent mainland,
1975-1980. See Figure 7-1 for locations of locality groups.
Localities
1. Lutz
2. Barbour-Hood
3. Shannon-AMNH
4. Shannon-Balboa
5. Lake-Wheeler
6. Barbour Stream
7. Miller Ridge
8. Fuertes
9. Conrad
10. Plateau
11. Drayton End
12. Armour End
13. Zetek 21
14. Standley Ridge
15. Standley End
16. Orchid Island
17. Gross Point
18. Chapman
19. Harvard
20. Mona Grita Point
21. Gigante
22. Frijoles Road
23. Bohio
24. Buena Vista
25. Pena Blanca
(A)
Total
individuals
5309
640
730
165
156
234
2499
1189
578
1377
138
456
146
786
649
249
145
388
125
40
140
156
746
143
138
(B)
Total
other-captures
1567
233
305
65
67
57
899
421
239
524
23
92
37
248
142
66
48
111
30
4
13
2
126
39
33
(B/A)
Percent
other-captures
30
36
42
39
43
24
36
35
41
38
17
20
25
32
22
26
33
29
24
10
9
1
17
27
24
Mona Grita Point, 10%; Gigante, 9%; and Frijoles Road, 1%).
These values show that more of the population was marked and
a larger portion of the area frequented was sampled at the
central localities. Bats moving in any direction from the central
localities were likely to encounter other capture stations. Bats
using the more isolated lakeshore localities probably foraged
extensively on the mainland; hence, we sampled smaller
fractions of their populations and the areas that they frequented.
The effects of sampling small fractions of populations and their
foraging areas are best seen on the mainland where stations
were few and (except for Bohio) capture effort was low. We
often netted at Bohio and it ranked sixth in numbers of A.
jamaicensis caught. However, Bohio was nineteenth in the
number of other-captures (17%, Table 7-2) and 83% of its A.
jamaicensis were caught only once.
The lowest other-capture rates (Table 7-2) on BCI were at
Drayton End (17%) and Armour End (20%). Among the most
isolated BCI stations, and located in high, old forest containing
few fruit trees, each of these two sites is over a kilometer from
the next nearest station. Bats at the southern perimeter of BCI
may forage on the adjacent mainland where the forest is
younger and contains many fig trees. Among the few recaptures
at Gigante and Mona Grita Point on the mainland were Armour
End and Drayton End bats.
At the outset of the Bat Project we gridded BCI and planned
to randomly net that grid. This plan was based on the
perception that good (representative) catches night after night
would result if we moved at random through our grid, using
well-sited and well-set nets at choice netting stations. Our
presumption was naive; on some nights we caught almost
nothing, whereas on other nights we were overwhelmed with
bats.
It became obvious that the nightly distribution of fruit bats
was not random, but coincided with the presence of ripe fruit,
which tends to be unevenly distributed in time and space. Nets
set at certain fruiting trees caught bats, nets placed elsewhere
often did not, and a locality might have an abundance of bats on
one date and few on another. When there was only one
preferred tree with ripe fruit on BCI, clearly that was the place
to be for bats. There are many factors that influence the
distribution and movements of fruit bats on BCI: distribution
and abundance of preferred foods; rain, wind, moon phase, and
cloud cover; the size, topography, and other limitations of
insularity. These factors tended to overwhelm our efforts to set
up meaningful measures of capture effort involving time and
netting conditions.
94 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 7-3.?Percentages of other-captures of Artibeus jamaicensis for selected locality groups on BCI weighted
by the number of total captures of A. jamaicensis at each of the locality groups where the other-captures were
recorded. Adjusted percentages were derived by dividing the number of other-captures (data from Table 7-1) by
the number of total captures for that locality group and reducing that value to a percentage of its column total. The
name of each locality group analyzed is followed by the total number of other-captures in parentheses.
Locality
group
1. Lutz
2. Barbour-Hood
3. Shannon-AMNH
4. Shannon-Balboa
5. Lake-Wheeler
6. B arbour Stream
7. Miller Ridge
8. Fuertes
9. Conrad
10. Plateau
11. Drayton-End
12. Armour-End
13. Zetek 21
14. Standley Ridge
15. Standley End
16. Orchid Island
17. Gross Point
18. Chapman
19. Harvard
20. Mona Grita PL
21. Gigante
22. Frijoles Road
23. Bohio
24. Buena Vista
25. Pena Blanca
Total
Total
captures
5309
640
730
165
156
234
2499
1189
578
1377
138
456
146
786
649
249
145
388
125
40
140
156
746
143
138
17,322*
Shannon-
AMNH (305)
%
6.35
8.06
10.04
11.51
6.95
1.17
2.71
1.60
2.82
10.26
9.82
1.79
1.87
1.38
0.84
3.28
1.87
7.00
8.68
1.98
Chapman
(110)
%
3.51
18.86
8.28
3.34
2.36
0.44
2.30
2.85
1.59
3.95
1.12
0.71
0.82
2.19
19.79
26.32
1.48
Other-captures
Lutz
(1567)
%
7.09
9.71
8.60
6.75
7.52
6.77
5.39
3.50
4.87
6.09
2.55
1.03
4.02
2.46
1.17
2.36
4.45
4.99
4.69
1.47
0.84
0.79
1.64
1.27
Miller
Ridge (899)
%
6.05
2.74
3.35
3.55
10.02
1.25
6.60
11.50
14.04
7.02
0.70
3.00
4.01
6.34
2.70
3.13
7.41
0.51
2.34
2.35
0.68
0.70
Standley
End (248)
%
1.25
1.49
1.29
9.20
3.45
4.46
1.68
1.72
9.82
16.48
28.80
1.92
1.25
7.04
6.71
3.45
* 15,736 band numbers.
Also, we had to adjust (prorate) capture rates because the
capture effort differed among localities. We tried "recaptures
per net-night" and "recaptures per net-hour," but these gave
anomalous results, probably because netting effort commonly
was inversely related to capture success. In other words, the
poorer our catch, the more nets we maintained and the longer
we worked them.
After realizing that capture effort measured in units of time
was unreliable, we discovered that the numbers of A.
jamaicensis caught per locality provided us the simplest and
most useful measure of capture effort. A. jamaicensis regularly
made up about two-thirds of our catch and was usually the
commonest bat anywhere we netted. Our accumulated 17,322
mark and recapture records of this species varied between
localities from a maximum of 5309 bats in the Lutz Watershed
to a minimum of 40 at Mona Grita Point (Table 7-3). Using
capture data from A. jamaicensis (Table 7-1), we derived
weighted percentages of other-captures by dividing the number
of other-captures at a locality group by the total number of A.
jamaicensis recorded at that same locality group. Each value
was then converted to a percentage of its column total to
produce the A. jamaicensis-'weighted percentages plotted in
Figures 7-3 through 7-8.
The efficacy of these methods for illustrating dispersion of
other-capture records of A. jamaicensis around a sample center
can be seen by comparing resulting percentages with the
distance between each capture locality and the center (Table
7-4). When graphed (Figure 7-9), the data points approximate
a line declining with increasing distance to zero indicating that
the frequency of other-captures was proportional to distance
from the sample center.
Another way we examined the correspondence of frequency
of other-captures with distance from the sample center was by
plotting the adjusted values on a map containing concentric
circles with radii of 1, 2, and 3 km from the sample center
(Figure 7-4). The Shannon-AMNH data fit rather well
NUMBER 511 95
45 46 47 48 49 50 51 52 53 54 55
i . ? ? 1 1 . . , ,
1 2 3 4 5
kilometers
FIGURE 7-3.?Other-captures of individual Artibeus jamaicensis recorded at least once in the Shannon-AMNH
locality group on BCI, 1976-1980 (expressed as a percentage of total other-captures of Shannon-AMNH bats and
weighted by A. jamaicensis capture means; data are from Table 7-3; Shannon-AMNH is outlined with a hexagon).
Isolines arbitrarily enclose locality groups with similar percentages of other-captures. Innermost line encloses
core area. Marginal numbers identify kilometer squares (see Appendix, Methods of Capturing and Marking
Tropical Bats).
96 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
47
46
45
45 46 47 48 49 50 51 52 53 54
? * ? ? i
1 2 3 4 5
kilometers
FIGURE 7-4.?Other-captures of individual Arlibeus jamaicensis recorded at least once in the Shannon-AMNH
locality group on BCI, 1976-1980 (expressed as a percentage of total other-captures of Shannon-AMNH bats and
weighted by A. jamaicensis capture means). Circles at one- and two-kilometer intervals encompass 29% and 85%,
respectively, of all other-captures. Shannon-AMNH is outlined with a hexagon.
NUMBER 511 91
4 7
4 6
4 5
1 . , ,
2 3
kilometers
FIGURE 7-5.?Other-captures of individual Artibeus jamaicensis recorded at least once in the Chapman locality
group on BCI, 1976-1980 (expressed as a percentage of total other-captures of Chapman bats, and weighted by
A. jamaicensis capture means). Chapman is outlined with a hexagon. Isolines arbitrarily enclose locality groups
with similar percentages of other-captures. Innermost line encloses core area. Marginal numbers identify
kilometer squares (see Appendix, Methods of Capturing and Marking Tropical Bats).
98 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
5 5
5 4
? ? ? ? ? '
2 3
kilometers
FIGURE 7-6.?Other-captures of individual Artibeus jamalcensis recorded at least once in the Lutz locality group
on BCI, 1976-1980 (expressed as a percentage of total other-captures of Lutz bats, and weighted by A.
jamaicensis capture means). Lutz is outlined with a hexagon. Isolines arbitrarily enclose locality groups with
similar percentages of other-captures. Innermost line encloses core area. Marginal numbers identify kilometer
squares (see Appendix, Methods of Capturing and Marking Tropical Bats).
99
4 5
1 . . . .
2 3
kilometers
FIGURE 7-7.?Other-captures of individual Artibeus jamalcensis recorded at least once in the Miller Ridge
locality group on BCI, 1976-1980 (expressed as a percentage of total other-captures of Miller Ridge bats, and
weighted by A jamaicensis capture means). Miller Ridge is outlined with a hexagon. Isolines arbitrarily enclose
locality groups with similar percentages of other-captures. Innermost line encloses core area. Marginal numbers
identify kilometer squares (see Appendix, Methods of Capturing and Marking Tropical Bats).
100 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
55
54
53
52
51
50
49
48
47
46
45
45 46 47 48 49 50 51 52 53 54 55
1
 ? ? ? ? ' ? '??
kilometers
FIGURE 7-8.?Other-captures of individual Artibeus jamaicensis recorded at least once in the Standley End
locality group on BCI, 1976-1980 (expressed as a percentage of total other-captures of Standley End bats, and
weighted by A. jamaicensis capture means). Standley End is outlined with a hexagon. Isolines arbitrarily enclose
locality groups with similar percentages of other-captures. Innermost line encloses core area. Marginal numbers
identify kilometer squares (see Appendix, Methods of Capturing and Marking Tropical Bats).
NUMBER 511 101
TABLE 7-4.?Measures of dispersal of Artibeus jamaicensis caught at least once at Shannon-AMNH. See Figure
7-1 for locality group locations.
Locality group
3. Shannon-AMNH
4. Shannon-Balboa
2. B arbour-Hood
11. Drayton-End
10. Plateau
1. Lutz
19. Harvard
5. Lake-Wheeler
18. Chapman
6. B arbour Stream
9. Conrad
7. Miller Ridge
20. Mona Grita Pt.
8. Fuertes
12. Armour-End
17. Gross Point
13. Zetek 21
14. Standley Ridge
16. Orchid Island
21. Gigante
15. Standley-End
24. Buena Vista
23. Bohio
25. Pena Blanca
22. Frijoles Road
Distance*
0
0.6
1.0
1.1
1.1
1.2
1.3
1.3
1.4
1.8
2.0
2.1
2.3
2.4
2.5
2.8
2.9
3.2
3.3
3.4
3.5
3.9
4.8
5.2
6.2
Total (unweighted)
Nf
27
7
19
5
51
124
4
4
10
1
6
25
0
7
3
1
1
4
3
0
2
0
0
1
0
%t
9
2
6
2
17
41
1
1
3
0.5
2
8
0
2
1
0.5
0.5
1
1
0
1
0
0
0.5
0
Other-captures
Percent
(A. jamaicensis
weighted)
10
12
8
10
10
6
9
7
7
1
3
3
0
2
2
2
2
2
3
0
1
0
0
2
0
Percent
(netting-night
weighted)
11
16
9
5
11
6
3
3
6
1
4
4
0
3
3
2
2
2
7
0
1
0
0
1
0
Percent
(net-hour
weighted)
10
16
12
5
8
7
4
3
8
1
3
4
0
3
2
1
2
1
9
0
1
0
0
0
0
* Distance in kilometers from Shannon-AMNH.
t Number of other-captures at each locality group of those individuals caught at least once at Shannon-AMNH.
t Other-captures of individuals recorded at least once at Shannon-AMNH (expressed as a percentage of total other-captures of Shannon-AMNH bats).
(compare Figures 7-3 and 7-4), with 29% of the localities
within 1 km, 85% inside 2 km, and 93% within 3 km of the
sample center.
Core Areas
Maps showing other-captures of bats taken at Chapman (an
eastern locality; Figure 7-5), Lutz (an east-central locality;
Figure 7-6), Miller Ridge (a west-central locality; Figure 7-7)
and Standley End (a western locality; Figure 7-8) reveal little
difference among the outlines of maximum extent of move-
ments. Given sufficient time and a large enough sample of
records, we suspect that bats of any locality on BCI could be
caught at every other locality on the island as well as on the
mainland. However, the decline of other-captures with distance
in each data set (Figures 7-4 and 7-9) shows that the population
of A. jamaicensis on BCI is not an amorphous, unstructured
mass of mobile bats that fly randomly throughout the island.
However mobile, individuals were more likely to be found in a
particular part of the island than elsewhere.
The mapped distributions of other-captures (Figures 7-5
through 7-8) each contain a central locality whose records were
analyzed for dispersion. Each map has three concentric isolines
around the central locality, enclosing all localities with
other-captures of bats caught at the central locality. The focal
localities of the four core areas (Figures 7-5 through 7-8;
combined in Figure 7-10) are spaced at intervals of about 1.5 to
2 km from east to west across BCI. Although the eastern
(Chapman) and western (Standley End) core areas are smaller,
the core areas overlap each other to a similar extent.
The smaller sizes of the Chapman and Standley End core
areas most likely resulted from undersampling the mainland
parts of their ranges. The area bound by the second isoline
(88% of other-captures) of Standley End (Figure 7-8) includes
several points on the mainland, but much less of BCI than is
covered by the frequently used areas of Miller Ridge (Figure
7-7) and Lutz (Figure 7-6) populations. The Chapman (Figure
7-5) area of frequent use is almost as limited on BCI as the
102 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
40% i
(0
111
cc
Q.
<
o
GC
LU
li.
o
I-
z
ULJ
o
cc
LU
Q.
30%-
20%-
10%
O Raw data
? Weighted with A.J.
A W e i g h t e d w i t h n e t t i n g - n i g h t s
3 4
KILOMETERS
6
FIGURE 7-9.?Comparison of three methods of illustrating distribution of percentages of other-captures of
individual Artibeus jama ic ens is recorded at least once in the Shannon-AMNH locality group on BCI, and
captured again there and elsewhere, 1976-1980. The graph correlates frequency of other-captures with distance
from Shannon-AMNH at zero. Data points are from Table 7-4.
corresponding area of Standley End. We do not have records
from the northeastern corner of BCI and the mainland to the
east where we never netted.
The core areas of most of our capture localities are plotted in
Figures 7-11 through 7-13. The convoluted shapes of some of
the areas such as those of Orchid Island (Figure 7-11),
Shannon-Balboa (Figure 7-12) and Armour End (Figure 7-13)
are the products of inadequate sample sizes from some of the
localities within the core other than the central locality. When
the plotted core areas (Figures 7-1 through 7-13) are
superimposed, even disregarding Orchid Island, Shannon-
Balboa, and Armour End because of incomplete sampling,
there is little of BCI left outside of a core area. Ten cores
overlap the Lutz core, 12 overlap the Plateau core, and 13
overlap the Miller Ridge core.
Although the central localities of Lutz, Barbour-Hood, and
Shannon-AMNH are close together (each about a kilometer
from the other) and their core areas overlap (Figure 7-11), each
seems to represent a slightly different group ofA.jamaicensis.
In contrast, the core areas of Fuertes, Conrad, and Miller Ridge
are neatly nested as though they all represented the same group
of bats (Figure 7-13).
Perhaps the most discrete units in the population of A.
jamaicensis on BCI are the harem groups permanently based in
tree holes. The bats netted at a particular locality would be
expected to include those that have day roosts there, those that
come to forage, and those that pass by enroute between day
roosts and feeding areas elsewhere. Discreteness of core areas
may distinguish among these bats.
We compared the percentages of other-captures at each
NUMBER 511 103
4 8
4 6
4 5
1 2 3 4 5
kilometers
FIGURE 7-10.?Overlap of core areas shown in Figures 7-5 through 7-8.
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
4 6
4 5
45 46 47 48 49
i . . . ? i
0 1 2 3 4 5
kilometers
FIGURE 7-11.?Overlap of core areas on the East-central and peripheral portions of BCI. GP = Gross Point; L =
Lutz; OI = Orchid Island; SA = Shannon-AMNH; TBH = Thomas Barbour-Hood; Z = Zetek.
NUMBER 511 105
5 5
5 4
5 3
5 2
5 1
5 0
4 9
4 8
4 7
4 6
4 5
45 46 47 48 49 50 51 52 53 54
2 3
kilometers
FIGURE 7-12.?Overlap of core areas in central and peripheral portions of BCI. BS = Barbour Stream; LW
Lake-Wheeler, P = Plateau; SB = Shannon-Balboa; SE = Standley End; SR = Standley Ridge.
106 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
49 50 514 5 46 47
? ? ? " '
0 1 2 3 4 5
kilometers
FIGURE 7-13.?Overlap of core areas in West-central and peripheral portions of BCI. A = Armour End; BO =
Bohio; B V = Buena Vista; CH = Chapman; C = Conrad; D = Drayton End; F = Fuertes; MR = Miller Ridge; PB
= Pena Blanca.
NUMBER 511 107
TABLE 7-5.?Core areas on BCI and vicinity in which the central locality had
a lower percentage of other-captures (see text for explanation) of Artibeus
jamaicensis (captured at least once there) than some other localities in the core.
Each entry includes the central locality (CAPITALIZED), percentage of
other-captures* there, rank among all localities in terms of number of
individual A. jamaicensis caught, and percentages of other-captures* at other
localities within the core. * = A. jamaicensis-v/eighled.
Locality
LUTZ
Barbour-Hood
Shannon-AMNH
Lake-Wheeler
Barbour Stream
Shannon-Balboa
MILLER RIDGE
Fuertes
Lake-Wheeler
Conrad
Gross Point
Standley Ridge
Plateau
PLATEAU
Shannon-Balboa
Shannon-AMNH
Conrad
Lake-Wheeler
Miller Ridge
Armour-End
FUERTES
Miller Ridge
Conrad
BOHIO
Pena Blanca
Buena Vista
SHANNON-AMNH
Shannon-Balboa
Plateau
Drayton-End
BARBOUR-HOOD
Chapman
Harvard
Shannon-AMNH
Barbour Stream
CONRAD
Plateau
Miller Ridge
Fuertes
Standley Ridge
ARMOUR-END
Mona Grita Point
Shannon-Balboa
CHAPMAN
Harvard
Barbour-Hood
ORCHID ISLAND
Gross Point
Buena Vista
Shannon -Balboa
Zetek21
SHANNON-BALBOA
Orchid Island
GROSS POINT
Orchid Island
Total
captures
5309
2499
1377
1189
746
730
640
578
456
388
249
165
145
Percent
other-captures
7
10
9
8
7
7
7
11
10
14
7
6
7
6
14
12
11
8
7
6
13
14
11
16
27
18
10
11
10
10
11
24
14
11
10
10
15
13
12
11
13
15
12
20
26
19
9
44
15
10
9
14
19
t
70
Rank
1
2
3
4
6
7
9
10
11
12
13
15
19
TABLE 7-6.?Core areas on BCI and nearby mainland in which the central
locality had a higher percentage of other-captures (see text for explantion) of
Artibeus jamaicensis (captured at least once there) than other localities in the
core. Each entry includes the central locality (CAPITALIZED), percentage of
other-captures* there, rank among all localities in terms of number of
individual A. jamaicensis caught, and percentages of other-captures* at other
localities within the core. * = A. jamaicensis-weighted.
Locality
STANDLEY RIDGE
Standley-End
Conrad
STANDLEY-END
Standley Ridge
Zetek 21
BARBOUR STREAM
Lake-Wheeler
LAKE-WHEELER
Barbour Stream
Miller Ridge
Gross Point
ZETEK 21
BUENA VISTA
DRAYTON-END
PENA BLANCA
HARVARD
Chapman
Total
captures
786
649
234
156
146
143
138
138
125
Percent
other-captures
23
14
10
29
16
10
36
18
26
12
10
10
42
82
31
84
49
24
Rank
5
8
14
16
18
20
22
23
24
t No other-captures recorded.
locality within each core (Tables 7-5 and 7-6). Percentages of
other-captures at the central localities ranged from 6% to 84%.
The lower percentages at Lutz, Miller Ridge, and Plateau must
reflect the numbers of captures, which were highest at these
three localities. If other-captures at a central locality are
predominantly local residents, their representation out of all
bats caught at that locality will be inversely related to the total
number caught. The greater the number of individual bats
involved, the greater the likelihood that other-captures will be
widely dispersed, thus also reducing the proportion of
other-captures at a central locality.
The high percentages of other-captures at Buena Vista and
Pefia Blanca simply demonstrate fidelity to those sites, which
are day roosts in channel markers. Whenever we sampled these
roosts, most of the bats caught were ones taken there before.
The low percentages of these bats netted away from their day
roosts suggest that they foraged where we did not net, probably
on the mainland. A comparison of the Bohio core area (Figure
7-13) and the Standley End area of frequent use (Figure 7-8)
shows that while these are places where Buena Vista and Pefia
Blanca bats foraged, they are probably not their main feeding
areas. There are extensive areas of the mainland near these
roosts where we have never netted (Figure 7-13).
There is a dichotomy of core areas into those whose central
localities have both lower percentages and fewer other-captures
than other localities in the core (Table 7-5) and those whose
central localities have higher percentages and more other-
captures than do neighboring localities (Table 7-6). This
division may be correlated with the number of captures.
108 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
60
55
50
45
40
I-
Z 35
LJLJ
O 30
cc
m 25
20
15
10
5
Number of individuals in each capture category
1
5061
57
2
2163
24
3
949
11
4
417
5
5
171
2
6
81
1
7
44
0.5
8
15
0.2
Number of records in each
1
5061
32
2
4326
28
3
2847
18
4
1668
11
5
855
5
6
4 8 6
3
7
308
2
8
120
1
9
4
0.04
10
1
0.01
capture
9
36
0.2
10
10
0.01
11
1
0.01
Total
8907
category
11
11
0.01
15728
5061 .
8907
5061
15728
I 0.57
I 0.32
Individuals
3 4 5 6 7 8
CAPTURE CATEGORY
10 11
FIGURE 7-14.?Frequency of capture of Artibeus jamaicensis on BCI. Number of individuals caught 1, 2, 3, 4,
and more times, and number of records in suites of individual bats in each capture category.
Standley Ridge and Standley End (Table 7-6) are exceptions in
that comparatively high numbers of A. jamaicensis were caught
at each (they ranked fifth and eighth, respectively), yet their
numbers of other-captures are also relatively high (see
discussion of Fidelity, below, in this section).
The distribution of fig trees probably exerts an influence on
the relative numbers of other-captures at any locality. The first
seven localities in Table 7-5 (Lutz through Barbour-Hood)
have an abundance of fig trees. Combined, Lutz and Miller
Ridge have over 200 fig trees, mostly Ficus insipida, the
favored fruit of A. jamaicensis. Chapman, Standley Ridge, and
Standley End have a fair number of fig trees, but not many F.
insipida. The other localities in Tables 7-5 and 7-6 have few fig
trees other than stranglcr figs (mainly F. obtusifolia) whose
fruits arc not preferred by A. jamaicensis.
If the number of A. jamaicensis harems is limited by the
availability of suitable tree holes, and if trees with suitable
holes are evenly distributed over BCI then there must be many
harem roosts that are not near patches of fig trees. At these
places we should catch the bats of resident harems and few
others, thus accounting for high percentages of other-captures
characterizing those sites. The bats of day roosts not located
near fig trees must routinely travel to other parts of the island to
feed. However, bats with day roosts near fig trees also commute
to other localities to forage whenever the trees near their roosts
lack ripe fruit. Nevertheless, these bats need to travel less than
bats residing in tree holes in fig-poor places. Turner (1975)
showed that Desmodus rotundus routinely changed roost sites
to remain close to a spacially shifting resource. We assume that
either roosting sites are limited on BCI or that A. jamaicensis
have high fidelity to individual day roosts because we found no
evidence of routine shifts even among bachelor males.
Bachelor males roost in foliage and not in tree holes.
Although they might be expected to concentrate in fig-rich
areas and to shift concentrations to follow fruit availability,
they apparently do not, judging by the unusually high ratio of
males consistently found at Standley End.
NUMBER 511
50
# 40-
Q
a 30 H
109
o
CO
<
CD
20-
10
0-
19
1 2
6%
20-
29
2 9
1 5 %
30-
39
3 6
1 9 %
40-
49
4
2%
50-
59
8 0
4 2 %
60-
69
9
5%
70-
79
3
2%
80-
99
0
1 0 0
1 7
9%
I I I 1 I I I I
0-19 20-29 30-39 40-49 50-59 60-69 70-79 80-99
CAPTURE CATEGORIES (%)
100
FIGURE 7-15.?Fidelity of Artibeus jamaicensis to the Chapman locality group on BCI. Frequency of capture of
individual bats with records of multiple captures that were caught at least once at Chapman are graphed as
percentages of records in various fractional capture categories ('/6 or less of records = 0%-19%, Vs-V*
= 20%-29%, V3 = 3O%-39%, 2/s = 40%-49%, lh = 50%-59%, Vs-Vi = 60%-69%, 3A = 70%-79%. 4 /s-
5/6 = 80%-99%, all = 100%). Row A in the table lists fractional capture categories (as percentages), row B lists
number of individual bats whose records at Chapman fall into each category (n = 190), and in row C the numbers
are converted to percentages. See also Table 7-7.
Fidelity
We examined fidelity to a particular locality group by
analyzing suites of multiple capture records of individual bats.
For each locality group we compiled records of all A.
jamaicensis having multiple captures that were taken at least
once in that particular locality group between October 1976 and
October 1980. For each bat, we tabulated total captures, the
number of captures in that particular locality group, and
percentage of its total records in that locality group. From that
tabulation we grouped those having multiple captures accord-
ing to the percentage of their occurrence at that locality group
among total records (e.g., Chapman, Figure 7-4).
The distribution of records among fractional categories is
influenced by the number of records per individual suite. In all,
3846 A. jamaicensis were recaptured (Figure 7-14). Most
(57%) were recaptured only once (i.e., had two captures), 24%
were recaptured twice (three captures), 11% recaptured three
times (four captures), and 8% recaptured four or more times.
Thus, peaks would be expected (Figure 7-15) at 50% and 100%
for two-record suites; 33%, 66%, and 100% for three records;
and 25%, 50%, 75%, and 100% for four records, and so forth.
Because most recaptured bats were caught again only once,
50% and 100% peaks per locality should occur most often.
These data indicate fidelity to a particular locality group.
High fidelity means a high frequency of records in the
60%-100% interval, which represents 3/s, 2/3,3A, 4/s, or more
captures in the same area. The hiqher the frequency of
same-site captures, the higher the fidelity. Low fidelity is
revealed by a higher frequency of records in the 0%-40%
interval (2/s, lfr, !/4, Vs, and !/6 of captures or less) for that
locality group. A simplified summary (Table 7-7) of locality-
group fidelity, like that in Figure 7-15, shows three basic
patterns among our data.
Pattern I (e.g., Armour End; Figure 7-16, Table 7-7) covers
most of the locality groups. There is a strong similarity among
110 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
? ? Ov O
tn l^  oo vd
-^  co ?
oo >n so so r-
f r~ ts oo >/?> oo
? N f /I -
-^~* SO ?* CO ^^ CO ^^
? ? co r- co
I g
NUMBER 511
60-
50
111
o
cc
0.
<
o
CO
<
00
40-
30-
20-
10-
0 J
"O = Chapman
? ? ? Conrad
A - Fuertes
?A ' Orchid Island
0-19 20-29 30-39 40-49 50-59 60-69 70-79 80-99
CAPTURE CATEGORIES (%)
FIGURE 7-16.?Fidelity of Artibeus jamaicensis to Pattern I locality groups on and near BCI: Chapman, Conrad,
Fuertes, and Orchid Island. See Figure 7-15 for further explanation.
1 0 0
the capture-category tabulations for locality groups with this
pattern in spite of their diverse locations and the disparity in
numbers in each suite of multiple capture records (from 51 to
1321). These locality groups share a low degree of fidelity
(<19% in the 60%-100% column) and a high frequency of
single captures (82%-99% in the 0%-40% and 0%-50%
columns).
Pattern II (Lutz, Bohio, and Standley End; Figure 7-17,
Table 7-7) comprises three seemingly unrelated locality groups
whose records of fidelity are remarkably similar. All three
show higher fidelity, compared with the Pattern I locality
groups (30%-32% in the 60%-l00% column), and fewer
single records (68%-70% in the 0%-40% and 0%-50%
columns). Their records may be similar for different reasons.
We sampled little of the probable foraging range of the Bohio
bats, so they had little risk of capture except at Bohio, thereby
appearing to have high fidelity to that location. In contrast, the
bats of Standley End may actually be sedentary because they
were recaptured mostly at Standley End or nearby (see Figure
7-8 and discussion of Core Areas earlier in this section). Or, if
we sampled only part of their foraging areas, the situation at
Standley End may be similar to that at Bohio.
We are confident that we have sampled the full extent of the
foraging ranges of Lutz bats. High fidelity to Lutz may reflect
a larger local resident population, or may result from catching
the same individuals repeatedly because of the attraction of the
fig grove in Lutz Ravine. These fig trees may adequately
support local populations of A. jamaicensis and periodically
attract bats from afar when ripe figs are scarce elsewhere. If this
is true then some of the bats showing high fidelity are actually
opportunistic transient foragers rather than Lutz residents.
Pattern III (Buena Vista and Pefia Blanca; Figure 7-18, Table
7-7) shows the highest fidelity. The obvious explanation for
this pattern is that we sampled only a fraction of the foraging
ranges of these bats, and because we captured them mostly at
their day roosts. We netted bats only at night at all other locality
groups and, evidently, we did not net where the bats of Buena
Vista and Pefia Blanca most often foraged.
The degree of fidelity within patterns appears to be related to
netting effort. On this basis we sorted Pattern I locality groups
112 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
50-|
40-
Q
c 30 -\
O
CD
20-
10-
0 J
O = B oh i o
? = Standley End
? = Lutz
I | ? ? ? ? ? ?
0-19 20-29 30-39 40-49 50-59 60-69 70-79 80-99
CAPTURE CATEGORIES (%)
FIGURE 7-17.?Fidelity of Artibeus jamaicensis to Pattern II locality groups on and near BCI: Bohio, Lutz, and
Standley End. See Figure 7-15 for further explanation.
1 0 0
into two subpatterns (Table 7-8). One with 19 or more
netting-nights per locality (subpattern la); the other with fewer
(subpattern Ib). With few exceptions (low fidelity at Conrad
and Lake-Wheeler; unusually high fidelity at Drayton End),
fidelity and netting effort within patterns are directly and
positively correlated, suggesting that the more often a locality
group is netted the more likely the bats using that locality group
will be recaptured.
Nevertheless, although netting effort differed greatly be-
tween subpatterns la and Ib, fidelity was similar. Therefore,
variation in fidelity between patterns is independent of netting
effort. Subpattern la localities were netted from 20 to 52 nights
and fidelity ranged from 7% to 18% (Table 7-8). Subunit Ib
localities were netted only 6 to 17 nights apiece, yet the fidelity
range was similar (8%-16%).
Fidelity was surprisingly similar (30%-32%) among pattern
II localities even though netting effort ranged from 14 nights at
Bohio to 197 at Lutz (Table 7-7). However, when comparing
fidelity on the basis of similar netting effort between patterns I
and II the results are markedly different. For example, 14
netting nights demonstrated 6% and 14% fidelity in Pattern I,
and 30% fidelity in Pattern II. Locality groups with 24 and 26
netting nights in Pattern I showed 9% and 13% fidelity;
whereas fidelity was more than double (31%) after similar
effort at Standley End (25 netting nights) in Pattern II.
If all bats having multiple captures that were recaptured only
once in a particular locality group are excluded, we should
eliminate most that were probably based elsewhere. Following
that logic, we considered A. jamaicensis captured two or more
times in a locality group more likely to be local residents. The
proportion of bats with two or more captures in a locality group
to the total multiple-capture cohort from that locality group
varied from 0.9% to 71.9%; although they still sorted into the
same patterns I, II, and III (Table 7-7). Few individuals caught
two or more times confirms low fidelity at locality groups such
as Conrad (11%) and Chapman (18%). The two-plus capture
fraction at Conrad may contain few local bats, judging from the
lower proportion (54%) of those bats in the 60%-100%
column. However, the high percentage (78%) in the 60%-
100% fractional capture category at Chapman indicates that the
two-plus fraction, although small, may represent mostly local
bats. The high proportion (78%) of bats at Pefla Blanca that
were caught there at least twice, and the high percentage (92%)
of those in the 60%-100% bracket, suggest that this exercise is
a valid means of estimating fidelity to a locality because high
fidelity is to be expected at a harem day roost.
NUMBER 511
50
w 4 0 -
Q
LU
cc 30
Q_
O 20 H
113
CO
CD
10-
0 J
Buenavista Light
Pena Blanca Light
I 1 1 1 " 1 1 ??i 1
0-19 20-29 30-39 40-49 50-59 60-69 70-79 80-99
CAPTURE CATEGORIES (%)
FIGURE 7-18.?Fidelity of Artibeus jamaicensis to Pattern III locality groups near BCI: Buena Vista and Pena
Blanca. See Figure 7-15 for further explanation.
100
We found that 102 (37%) of the 275 A. jamaicensis caught at
Standley End had been caught there at least twice (Table 7-7).
Of these, 83% fall into the 60%-100% recapture category for
the site. This is good evidence that a high proportion of the
Standley End bats were local residents, a conclusion further
supported when we examine their records in greater detail.
Only two (7%) of the two-plus females were caught as many as
two times elsewhere (at Bohio and Standley Ridge). Also, only
six (8%) of the males caught two or more times at Standley End
were caught as many as two times at other sites, all nearby
(Fuertes, 1; Miller Ridge, 8; and Standley Ridge, 2).
The sex ratio of the Standley End A. jamaicensis (102) is
skewed toward males (73 : 29; Table 7-9). At Lutz, another
Pattern II locality with similar fidelity statistics, the ratio is
53 :47. During three of the netting episodes at Standley End
when two-plus bats were caught, males outnumbered females
30 to 1. Of males caught at least twice, 31% were also caught
three or more times while only 14% of the females were caught
that often. In contrast, only 21 (29%) males were caught over a
relatively long period (two to four years), whereas 14 (48%)
females were recaptured at Standley End during the same
period. Close to three-fourths (71%) of the males were found
there for a year or less (Table 7-9). Age distribution among bats
captured two or more times was similar in males and females
(Table 7-10); however, a larger proportion of the young males
than young females stayed in the area to be caught later as
adults.
We believe that the males at Standley End were predomi-
nantly bachelors, and that most or all of the resident females
were members of harems. Of the 20 females caught as adults
during seasons of reproduction, 18 were pregnant, lactating, or
postlactating at one or more of the captures. The greatest
number of females caught as adults at Standley End in any half
year was 11. Presuming that we caught most of the resident
females, they probably represent from one to three harems. In
the four harems of A. jamaicensis that Morrison (1979) studied
on BCI, he found from four to 11 adult females (X= 6.5).
We still do not know why fidelity was so high in the three
Pattern II locality groups (Lutz, Bohio, and Standley End).
Incomplete coverage of foraging ranges may be a factor at
Bohio and Standley End, but not at Lutz, which is surrounded
by well-netted localities that have typical low Pattern I fidelity
percentages. Other peripheral locality groups such as Chapman,
Standley Ridge, and Armour End show low fidelity, suggesting
that peripheral location is not the reason.
114 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 7-8.?Fidelity of Artibeus jamaicensis to a particular locality on BCI,
ranked by number of netting nights. See Table 7-7 and text for explanation of
categories.
Locality
PATTERN la
(more than 19 netting nights)
Miller Ridge
Plateau
Fuertes
Shannon-AMNH
Barbour-Hood
PATTERNIb
(less than 19 netting nights)
Chapman
Standley Ridge
Barbour Stream
Conrad
Lake-Wheeler
Harvard
Armour End
Drayton End
Zetek21
Gross Point
Shannon-Balboa
Orchid Island
PATTERN II
Lutz
Standley End
Bohio
Rank
1
2
3
4
5
1
2
3
4
5
6
7
8
9
10
11
12
1
2
3
Netting
nights
52
46
26
24
20
17
16
14
14
12
11
11
10
6
5
4
4
197
25
14
60-100%
18
12
13
9
7
16
15
14
6
4
12
8
14
8
1
3
3
32
31
30
We suggest that the high capture rate at Lutz is correlated
with the unusual local abundance of fig trees. That also could
be true of Bohio because our netting there generally coincided
with the availability of ripe figs; however, fig trees were scarce
at Standley End. The abundance of fig trees at Miller Ridge
rivals that of Lutz, yet fidelity was low, as was typical of other
Pattern I locality groups. Geographically, the Pattern II locality
groups are dissimilar: Bohio is on the mainland, Standley End
is peripheral on BCI, and Lutz is more central. In terms of size,
Lutz encompasses the largest area, and because of its proximity
to the Laboratory Clearing, it received the greatest sampling
effort. Lacking a better explanation, one could argue that the
similarities in capture frequency among the locality groups in
Pattern II are merely coincidental.
Movements of Individual Bats
Thus far we have discussed movements of bats associated
with a particular locality group based on pooled data. We also
examined the movements of individuals captured at two or
more localities away from the central locality under considera-
tion. To illustrate this we have mapped the movements of five
female A. jamaicensis from Pefia Blanca (Figure 7-19). Each
female was caught at two or more localities away from the light
tower, and polygons outlining the locations where each was
captured approximate their known home ranges. We then
overlaid this map (Figure 7-19) with a 0.5 km grid and counted
the number of times individual polygons touched each square.
The resulting map (Figure 7-20) shows the frequency (from one
to five) of occurrence of individual bats in each of the squares.
We also mapped the same kind of information from 11 bats of
the day roost in the Buena Vista light tower (Figure 7-21).
This method proved effective for illustrating movements
TABLE 7-10.?Age distribution of Artibeus jamaicensis captured two or more
times at Standley-End, BCI.
Sex
Female
Male
Caught only
when young
Caught first as young
later as adult
Caught only
as adult
14%
6%
38%
49% 45%
Sex
FEMALE
number
percent
MALE
number
percent
TABLE 7-9.?Sexual variation in age,
or more times at Standley-End, BCI.
N J-S
29
73 1
1
Age during
capture span
J-A SAD
3 4
10 14
11 4
15 6
S-A
8
28
24
33
capture span, and number of captures of Artibeus jamaicensis caught two
AD
14
48
33
45
1
15
52
52
71
Capture span
(years)
2 3
7 4
24 14
48%
13 7
18 10
29%
4
3
10
1
1
Number of captures
at Standley-End
2
25
86
50
68
3 4 5+
3 1
10 4
14%
14 8 1
19 11 1
31%
2
11
38
31
42
Total
captures
3
9
31
20
27
4
8
28
10
14
5
1
3
8
11
6+
4
5
NUMBER 511 115
4 5
i . ? ? ? i . . . .
2 3
kilometers
FIGURE 7-19.?Movements of five female Artibeus jamaicensis from the day roost in the Pena Blanca light tower
to BCI and other nearby areas.
116 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
4 6
4 5
? ? ? ? ? ? ? ? ? ? '
2 3
kilometers
FIGURE 7-20.?Frequency of occurrence of five Artibeus jamaicensis from the day roost in the Pena Blanca light
tower in nearby 0.5 km squares.
NUMBER 511 117
5 5
5 4
5 3
5 2
5 1
5 0
4 9
4 8
4 7
4 6
4 5
52 53 5445 46 47 48 49 50
I . . . ?! . . . .
2 3 4
kilometers
FIGURE 7-21.?Frequency of occurrence of 11 Artibeus jamaicensis from the day roost in the Buena Vista light
tower in nearby 0.5 km squares.
118 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
even though it only approximates the area these bats use. If the
average longevity of an A. jamaicensis on BCI is about two
years (see Section 5, Survival and Relative Abundance, Figure
5-8), the average bat can be expected to fly on about 700 nights
during its life. Nevertheless, we have recorded an average of
only 1.8 captures per individual and a maximum of 11
captures?a small glimpse into the lives of these bats.
Mobility
There are few references in the literature on the distances that
A. jamaicensis moves. Based on actual distances determined by
radio tracking between day roosts and foraging sites, these bats
are known to travel (one way) up to a kilometer (0.6 ? 0.4 km,
n = 17) on BCI to as far as 10 km (8 ? 2 km, n = 4) in Jalisco,
Mexico, in a single night (Morrison 1978b). The bats in the day
roosts in the canal-marker light towers also provided distances
from day roost to netting sites. Of course we have no way of
knowing whether a bat flew directly from the light tower to the
place it was caught, or came from some other location.
Nevertheless, based on the assumption that the bats moved
from day roosts in the canal markers to netting sites, the
average distances (Table 7-11) traveled by females from the
Buena Vista roost were: Adults, 1.64 km (n = 32); subadults,
2.68 km (n = 3); juveniles, 3.36 km (n = 3). The average
distances traveled by Buena Vista adult females is comparable
to foraging distances covered between day roosts and feeding
areas (1.6 km) by Costa Rican Carollia perspicillata as
reported by Heithaus and Fleming (1978). However, the Buena
Vista subadults and juveniles traveled considerably greater
distances. Also greater were average distances traveled by
female A. jamaicensis from the Pefla Blanca marker: Adults,
3.21 km (n = 13); subadults, 3.16 km (n = 3). A comparison
between Heithaus and Fleming's (1978) data for C. perspicil-
lata and ours for A. jamaicensis probably is not appropriate
because their data was based on radio telemetry and gathered
over a short period of time (up to 19 nights) during the wet
season. Because they used radio telemetry, distances between
roosts and foraging sites were more easily defined and
correspond more closely to Morrison's (1978b) commuting
distances. Fleming and Heithaus (1986) showed that seasonal
changes in food availability also influenced distances traveled
by C. perspicillata.We do not know what our A. jamaicensis
were doing or where they went between leaving their day roosts
and being captured.
We summarized the average distance between capture sites
by sex, age, and locality group based on 5542 records of
recaptures of A. jamaicensis at sites other than where the bats
were marked (Table 7-11). The distances traveled between
these sites, often recorded months apart, are not exactly
equivalent to Morrison's (1978b) commuting distances, which
were based on bats radio tracked during a single night. The
mean distances between captures (Table 7-11) do not seem to
be correlated with age or sex. Although a superficial
examination of the data suggests that patterns exist, closer
scrutiny failed to reveal any overall consistency.
Movements (Table 7-11) by adults outnumbered those of
subadults about 2 : 1, records of subadult females outnumbered
those of juvenile females by about 3 : 1 , and records of subadult
males outnumbered those of juvenile males by about 2 : 1 .
Although these ratios appear to reflect the relative duration of
these age categories in the population, ratios based on the
average number of months when an individual A. jamaicensis
can be captured as either adult, subadult, or juvenile are about
15 : 8 : 1. Proportionately, however, movements by juveniles
are much more frequent than expected, but those of adults are
as expected. This disparity may reflect greater ease of
recapturing juveniles. Although among records of movements
of adults and subadults, females outnumbered males, and in
movements of juveniles, males outnumbered females, this is
the relationship among all captures, so it is unlikely to be
significant as far as movements are concerned.
Even though the mean distances between captures seem to
show no correlation with age or sex (Table 7-11) they do show
a correlation with the average distance separating a capture
station from all other stations. This relationship is shown in
Figures 7-22 through 7-27 in which the mean distance between
captures has been plotted in each locality group. With the data
organized geographically, the distances traveled by females in
the core area are a little greater than corresponding distances for
males among both adults and juveniles. The distances flown are
greatest in subadults among males; but greatest in adults and
juveniles among females. Correlations between age and sex are
not evident outside the core area. Three distance records of
movements between Bohio and Armour End (5.93 km) are the
longest recorded between any captures. These two locality
groups are also the most distantly separated of any of the sites
where we frequently netted.
Nightly Movements
Radio-tracking showed that A. jamaicensis commonly visits
more than one tree in an evening (see Section 9, Foraging
Behavior). We have evidence of this when, for example, we net
a bat carrying a Ficus insipida fruit, but defecating seeds of F.
trigonata. This bat must have fed at a F. trigonata on the same
evening because food passage is much too rapid (we have
recorded food passage times of from 7 to 45 minutes; see
Section 2, Physiology) to claim that the seeds are from a fig
eaten on the previous night.
We tried to demonstrate movements between fruiting trees
on the same night by operating netting stations simultaneously
at several localities. Although we handled 1170 A. jamaicensis
on 13 of those nights (Table 7-12), we captured only one again
the same night at a different tree. This was a postlactating
female captured at 1900 h on 7 November 1979 near a F.
NUMBER 511 119
TABLE 7-11.?Mean distance (in kilometers) between actual points of capture of individual Artibeus jamaicensis
on BCI and the adjacent mainland summarized by locality group, sex, and age. Number in each sample in
parentheses.
Locality
Lutz
Barbour-Hood
Chapman
Harvard
Shannon-AMNH
Drayton End
Armour End
Zetek 21
Standley Ridge
Standley End
Fuertes
Miller
Gross Point
Barbour Stream
Lake-Wheeler
Shannon-Balboa
Plateau
Conrad
Orchid Island
Bohio
Buena Vista
Pena Blanca
Total n
JUV
1.13
(79)
1.25
(8)
0.95
(3)
1.28
(28)
2.81
(6)
1.75
(5)
1.25
(45)
1.34
(32)
0.95
(3)
1.42
(32)
2.21
(20)
2.83
(5)
3.36
(3)
269
Female
SAD
1.27
(364)
1.14
(35)
1.32
(14)
1.90
(5)
1.34
(69)
2.22
(17)
2.20
0D
1.29
(18)
2.59
(11)
1.23
(57)
1.21
(78)
2.01
(3)
0.77
(5)
0.80
(3)
1.07
(13)
1.39
(73)
1.72
(21)
2.07
(23)
3.82
(6)
2.68
(3)
3.16
(3)
832
AD
1.04
(574)
1.28
(84)
1.27
(38)
1.31
(15)
1.46
(77)
1.90
(11)
2.18
(25)
1.81
(26)
1.55
(57)
1.73
(63)
1.05
(138)
1.03
(248)
1.21
(17)
1.01
(71)
1.05
(31)
1.22
(18)
1.21
(209)
1.57
(56)
1.87
(60)
1.75
(62)
1.64
(32)
3.21
(13)
1925
JUV
0.93
(92)
0.86
(8)
1.30
(4)
1.28
(29)
2.97
(11)
2.56
(14)
1.50
(4)
1.42
(41)
1.23
(37)
0.83
(3)
0.72
(7)
1.32
(51)
2.24
(17)
2.35
(5)
4.18
(3)
326
Male
SAD
0.93
(302)
1.13
(23)
0.79
(3)
1.80
(4)
1.50
(48)
2.39
(4)
2.09
(18)
2.11
(7)
1.78
(44)
1.77
(22)
1.31
(32)
1.15
(50)
1.47
(3)
1.15
(9)
1.58
(3)
0.77
(3)
1.34
(88)
1.86
(18)
2.38
(13)
2.95
(7)
701
AD
0.91
(528)
1.22
(35)
1.55
(23)
1.61
(9)
1.23
(66)
1.89
(15)
2.41
(24)
1.77
(23)
1.46
(126)
1.84
(82)
0.92
(62)
1.01
(196)
1.15
(8)
1.42
(20)
0.92
(8)
1.07
(18)
1.31
(154)
1.71
(46)
1.85
(26)
2.05
(20)
1489
JUV
1.13:0.93
1.25:0.86
0.95:1.30
1.28:1.28
2.81:2.97
1.75:2.56
1.25:1.42
1.34:1.23
0.95:0.72
1.42:1.32
2.21:2.24
2.83:2.35
Ratio (female:male)
SAD
1.27:0.93
1.14:1.13
1.32:0.79
1.90:1.80
1.34:1.50
2.22:2.09
2.20:2.11
1.29:1.78
2.59:1.77
1.23:1.31
1.21:1.15
2.01:1.47
0.77:1.15
0.80:1.58
1.07:0.77
1.39:1.34
1.72:1.86
2.07:2.38
3.82:2.95
AD
1.04:0.91
1.28:1.22
1.27:1.55
1.31:1.61
1.46:1.23
1.90:1.89
2.18:2.41
1.81:1.77
1.55:1.46
1.73:1.84
1.05:0.92
1.03:0.61
1.21:1.15
1.01:1.42
1.05:0.92
1.22:1.07
1.21:1.31
1.57:1.71
1.87:1.85
1.75:2.05
insipida at Armour-Zetek Junction and netted again 1.2 km
away at 2100 h on the same evening near another fruiting F.
insipida at Miller 9.
Our failure to catch more bats moving between fruiting trees
on the same night may have stemmed from net avoidance
(adverse conditioning), from an unfortunate choice of inappro-
priate combinations of fruiting trees, or from low probability
because of the large number of bats involved (the "drop in the
bucket" principle).
When we netted the same place for two or more nights
because of the continued availability of ripe figs, and our
captures of A. jamaicensis averaged 25 or more per night (X =
120 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
45 46
2 3
kilometers
FIGURE 7-22.?Mean distance in kilometers between captures of adult female Artibeus jamaicensis on and near
BCI. Isolines enclose locality groups with similar mean distances and reflect distances between enclosed capture
stations and all other capture stations. See text for further explanation.
4 6
4 5
i . . . 11 . . . .
2 3
kilometers
FIGURE 7-23.?Mean distance in kilometers between captures of adult male Artibeus jamaicensis on and near
BCI. Isolines enclose locality groups with similar mean distances and reflect distances between enclosed capture
stations and all other capture stations. See text for further explanation.
122 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 7-24.?Mean distance in kilometers between captures of subadult female Artibeus jamaicensis on and
near BCI. Isolines enclose locality groups with similar mean distances and reflect distances between enclosed
capture stations and all other capture stations. See text for further explanation.
NUMBER 511 123
kilometers
FIGURE 7-25.?Mean distance in kilometers between captures of subadult male Artibeus jamaicensis on and near
BCI. Isolines enclose locality groups with similar mean distances and reflect distances between enclosed capture
stations and all other capture stations. See text for further explanation.
124 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
45 46 47 48 49 50 51 52 53 54 55
i . . . i i . . . .
0 1 2 3 4 5
kilometers
FIGURE 7-26.?Mean distance in kilometers between captures of juvenile male Artibeus jamaicensis on and near
BCI. Isolines enclose locality groups with similar mean distances and reflect distances between enclosed capture
stations and all other capture stations. See text for further explanation.
NUMBER 511 125
4 7
4 6
4 5
5 5
i . ? ? ? i . . .
0 1 2 3 4 5
kilometers
FIGURE 7-27.?Mean distance in kilometers between captures of juvenile female Artibeus jamaicensis on and
near BCI. Isolines enclose locality groups with similar mean distances and reflect distances between enclosed
capture stations and all other capture stations. See text for further explanation.
126 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 7-12.?Catches of Artibeus jamaicensis and other bats during episodes
of netting at two or more stations on the same night on BCI.
Date
29 Nov 78
HJun79
7 Nov 79
8 Nov 79
9 Nov 79
11 Nov 79
12 Nov 79
13 Nov 79
14 Nov 79
15 Nov 79
16 Nov 79
18 Nov 79
12 Oct 80
13 nights
Locality
Lutz Creek
Snyder-Molino 0-2
Barbour-Lathrop 16
Snyder-Molino 0-2
Miller 9
Armour-Zetek Jet.
Armour-Zetek Jet.
Armour-Conrad Jet.
Miller 9
Donato 3-4
Miller 1-2
Barbour3
Donato 3-4
Barbour 3
Snyder-Molino-Lutz
Standley 15
Standley 21
Miller 4-5
Standley 21
Lutz Creek
Donato 3-4
Standley 16
Donato 3-4
Standley 16
Standley 16
Donato 3-4
Miller 13-14
Miller 15
Miller 8-10
Chapman 6-9
30 sites
Artibeus
jamaicensis
26
56
109
6
77*
83*
2
27
11
47
19
24
42
27
5
10
6
2
10
1
94
103
14
68
23
42
56
30
101
49
1170
Other
bats
15
27
33
4
47
16
3
27
18
54
25
14
47
22
3
13
10
4
26
10
136
82
27
100
54
45
40
32
12
12
958
* One double capture.
60 for 128 nights; see Table 7-13), only 2% (range, 0%-6%) of
individual A. jamaicensis were captured more than once at the
same tree on successive nights. These recaptured bats were 5%
(range, 0%-13%) of all captures of A. jamaicensis, which
represents a pool of 7427 individuals amassed over 128 nights.
In all, only 181 were caught at the same tree on two successive
nights, and seven were captured on three successive nights.
Individual A. jamaicensis were caught more than once in 35 of
46 multinight netting episodes at single ripe trees.
The frequency of repeats (bats caught more than once in a
night at the same station) is similar to the frequency of
recaptures on successive nights. At least some A. jamaicensis
reentered a net within minutes of release, probably because of
disorientation resulting from the handling process and because
of proximity of the processing station to nets. Nevertheless, the
impression was that, once captured, these bats avoided the nets.
During sampling periods totaling 133 nights in 1979 and 1980
we had 158 repeats of A. jamaicensis on 59 nights; an average
of 2.7 repeats on the nights with repeats. On the nights with
repeats, we caught 4022 A. jamaicensis, 3.9% of which
represented repeated captures. Repeated captures represented
2.7% of all A. jamaicensis caught on all nights repeated (133
nights, 5946 bats).
If we could estimate the proportion of marked and unmarked
bats in a foraging aggregation we might be able to estimate the
number of A. jamaicensis that come to a fruiting tree. We know
that the recapture rate is low (<2%), but we do not know what
our success rate is in capturing unmarked bats. To judge from
the nightly ratio of unmarked to recaptured bats (Table 7-13),
these variables must be changing from night to night.
If we assume that many of the same bats return night after
night to a choice tree as long as fruit remains, and that we
recapture only a small fraction of marked bats, then a tally of
TABLE 7-13.?Results of netting episodes involving consecutive nights at single localities on BCI and the
adjacent mainland. The columns of capture records, multiple captures, and mean captures per night pertain to
Artibeus jamaicensis alone. The last column, total captures all species, includes A. jamaicensis and all other bats.
Date
Jan 78
Apr 78
Jun78
Nov 78
May 79
Nov 79
Dec 79
Apr 80
Oct 80
Total
Feb78
Scp79
Nov 79
Total
Nights
N
3
4
3
2
2
2
4
4
3
27
3
2
4
9
N
291
97
85
106
79
94
253
145
319
1469
99
83
109
291
Capture records
Marks
179
37
72
75
48
27
76
38
120
672
102
58
87
247
Recaps
117
63
16
32
32
67
182
109
208
826
201
141
196
538
Total
Multiple captures*
Individuals
N %
Records
N ?
Miller Ridge (9 multinight episodes)
296
100
88
107
80
94
258
147
328
1498
5
3
3
1
1
0
5
2
9
29
2
3
4
1
1
0
2
1
3
2
10
6
6
2
2
0
10
4
18
58
Standley Ridge (3 multinight episodes)
12
4
4
20
25
8
8
41
12
6
4
8
188
137
192
517
3
6
7
2
3
0
4
3
6
4
6
3
2
4
Mean
captures
per
night
99
25
29
54
40
47
65
37
109
56
67
71
49
60
Total
captures
all
all
species
529
148
132
150
140
179
321
273
402
2274
274t
205
448
927
NUMBER 511 127
TABLE 7-13.?Continued.
Date
Dec 78
Apr 79
Sep80
Oct80
Total
Jan 80
Aug80
Oct80
Total
Sep79
Oct79
Nov79
Aug80
Aug80
Total
Mar 78
Mar 78
Nov-Dec 78
Mar 79
Oct79
Oct79
Nov79
Nov79
Nov79
May 80
Aug80
Sep-Oct 80
Oct80
Total
Aug80
Dec 78
Sep79
Nov78
Sep80
Sep80
Apr 79
Apr 79
Apr 80
Total
Total for table
Nights
N
2
2
2
3
9
2
4
2
8
2
2
2
3
2
11
2
2
3
3
3
2
2
2
2
13
2
3
2
41
2
2
4
3
2
3
2
2
3
23
128
N
76
149
101
121
447
50
270
285
605
138
105
82
107
98
530
67
63
120
145
332
108
89
54
108
767
147
169
104
2273
147
99
326
86
199
283
165
151
130
1586
7427
Capture records
Marks
64
106
88
56
314
11
176
142
329
89
65
19
75
64
312
16
19
88
54
183
45
34
15
40
637
96
93
49
1369
93
52
225
70
100
203
163
147
113
1166
4453
Recaps
13
46
18
69
146
39
102
146
287
51
41
63
35
34
224
52
44
35
99
161
64
55
39
68
157
51
80
55
960
56
52
119
19
105
86
2
6
27
472
3162
Total
Multiple captures*
Individuals
N %
Records
N
Bohio (4 multinight episodes)
77
152
106
125
460
1
3
5
3
12
1
2
5
3
3
2
6
10
7
25
Fuertes (3 multinight episodes)
50
278
288
616
0
8
3
11
0
3
1
2
0
16
6
22
Plateau (5 multinight episodes)
140
106
82
110
98
536
2
1
0
3
0
6
1
1
0
3
0
1
4
2
0
6
0
12
Lutz (13 multinight episodes)
68
63
123
153
344
109
89
54
108
794
147
173
104
2329
1
0
3
8
12
1
0
0
0
27
0
4
0
56
2
0
3
6
4
1
0
0
0
4
0
2
0
3
2
0
6
16
24
2
0
0
0
54
0
8
0
112
Miscellaneous (9 multinight episodes)
149
104
344
89
205
289
165
153
140
1638
7615
Barbour-Hood
2
Chapman
5
1
5
RCS-AMNH
15 5
Lake-WMW
3
Conrad
6
4
3
Armour End
6 2
Orchid Island
0 0
Frijoles Road
2
Gigante
8
47
181
1
6
3
2
4
10
33
6
12
12
0
4
18
99
369
%
3
4
9
6
5
0
6
2
4
3
2
0
6
0
2
3
0
5
11
7
2
0
0
0
7
0
5
0
5
3
10
10
7
6
4
0
3
13
6
5
Mean
captures
night
39
76
53
42
51
25
70
144
77
70
53
41
37
49
49
34
32
41
51
115
55
45
27
54
61
74
58
52
57
75
52
86
30
103
96
83
72
47
71
60
Total
captures
all
species
160
177
156
176t
669
119
325
342
786
181
393
101
131
112
918
159
143
178
260
419
149
189
90
271
969
171
230
172
3400
170
134
419$
240
234
351
1%
220
224*
2188*
11162
* Individual A. jamaicensis captured two or more times during a multinight
netting episode.
t One caught three times.
X Three caught three times.
* Two caught three times.
? Seven caught three times.
128 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 7-14.?Large concentrations of Artibeus jamaicensis at single netting
stations on BCI on successive nights.
Locality
Miller Ridge
Shannon-AMNH
Lutz
Miller Ridge
Lutz
Fuertes
Armour End
Miller Ridge
Fuertes
Date
Jan 78
Sep79
Oct79
Dec 79
May 80
Aug80
Sep80
Oct80
Oct80
Nights
N
3
4
3
4
13
4
3
3
2
Artibeus
jamaicensis
N
291
326
332
253
767
270
283
319
285
Average
number per
night
99
86
115
65
61
70
96
109
144
the number of individuals captured during a multinight netting
sequence should suggest the number of bats that flock to a tree
(Table 7-14). We believe that, on occasion, these numbers must
be large, and even if we are catching only a third of the bats, the
total at a fruiting tree may exceed a thousand. Our usual
impression at the nets during a highly successful night is that
while the air seems full of bats, relatively few are getting into
the nets.
Group Movements
The number of bats at a netting station, especially if it is at an
active feeding roost near a fruiting tree, varies during the night,
usually abruptly. This is evidence that the bats are moving
about in groups. Whether these groups are associations of
individuals that forage together night after night (and could be
considered true flocks), or are merely aggregations of bats that
form at a feeding roost and shift together from one feeding site
to another during the night and then disband for indefinite
periods of time is not known.
There is no doubt about the existence of aggregations.
Anyone who has much experience working with mist nets in
the American tropics has to be impressed with abrupt and
dramatic shifts in numbers of bats during the night, signaling
the arrival and departure of groups. Heithaus et al. (1974)
commented that large bats appeared to arrive in groups to feed
and that visits by groups to food sources was pulsed. We refer
to these pulses as surges, and we define a surge as an abrupt
increase in numbers of bats captured, followed by an abrupt
decrease. When and whether there are surges depend on such
influences as rain, presence of ripe fruit, the amount of light,
and the phase of the moon. Our data on surges were compiled
for three-month periods at the height of the rainy season
(August-November) in 1979 and 1980 (n = 133 nights; means
summarized in Table 7-15).
Admittedly these data are biased and incomplete. On a night
with few bats we might stop netting after a few hours, thus
recording a night without a surge. On similar nights we
persisted, perhaps waiting for the moon to set and still did not
record a surge; or, had the first surge commence as late as
2300 h. We undoubtedly missed some second surges by
terminating too soon after the first. During the weeks of a full
and new moon, moonrise and moonset often coincided with the
beginning and end of surges.
Bats are least active in the week following the first quarter of
the moon (the week with most light in early evening). Captures
were few (average 35.4 per night), surges infrequent and short
(2.5 h), and only half of the nights had any surge at all (Table
7-15). Only 4% (one in 28 nights) had a second surge. The first
surge was early, beginning at approximately 1915 h and ending
at about 2045 h. Presence of fruit and absence of rain seemed to
be of relatively little consequence during nights with bright
moonlight.
In spite of increasing light in early evening, A. jamaicensis
was most active in the week following the new moon. Capture
rate was high (averaging 53.8 per night) and surges occurred on
80% of the nights. Probably because of the early evening light,
second surges occurred on 20% of the nights. The first surges
were of long duration, lasting about 3.5 h, and they began about
1945 h and ended near 2215 h. Morrison (1978a) used the term
lunar phobia to describe these correlations of activity and moon
phase.
Summary
The recapture rate in our 8907 A. jamaicensis averaged 1.8
per bat, indicating that less than 50% were recaptured at all, and
less than 20% were recaptured three or more times. The low
recapture rate, long distances between recapture sites, and
potential home ranges that include the entire island and parts of
the adjacent mainland complicate movement analyses. We
adjusted for some of these difficulties by pooling the data for
each locality.
We tabulated captures by species and by half years on a
matrix of locality groups and then summarized the entire
marking interval (October 1976 through October 1980).
Although neither factor completely explains the variation,
proximity of netting localities and differences in netting effort
led to recapture rates varying from 1 % to 43%. Localities in the
center of the island consistently yielded better recapture rates
than did marginal localities, suggesting that bats living near the
edge of the island also forage on the surrounding mainland. It
proved impractical to use netting sites randomly on a grid on
BCI. Capture success was influenced by rain, wind, cloud
cover, moon phase, topography, and the distribution and
abundance of preferred foods. Thus, we had to try to
standardize capture effort by the use of such measures as
recaptures per net-night, or net-hour. We settled on using the
number of A. jamaicensis caught per locality as the most useful
and effective measure of capture effort.
The population of A. jamaicensis on BCI is not an
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130 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
amorphous unstructured mass of mobile bats flying randomly
throughout the island. Individuals are more likely to be
recaptured close to where they were marked. Bats netted at a
particular locality include those that have day roosts in the area
as well as those coming to forage at fruiting trees, and those
caught as they travelled between day roosts and feeding sites
elsewhere. We believe that the distribution of fig trees is a
major influence on the relative number of recaptures at any
locality.
We examined fidelity to a particular area (locality group) by
analyzing suites of multiple capture records of the 3846 bats
recaptured and found three patterns. Highest fidelity occured
where we sampled day roosts, rather than foraging sites.
Fidelity is at least partially dependent upon netting effort. In
locality groups with unusually high fidelity, the sex ratio was
skewed toward males. In one such group, most of the males
were bachelors, and most of the females were members of
harems.
Data on movements of individual bats was restricted by the
relatively small number of multiple recaptures. The average bat
flies on about 700 nights during its lifetime, yet we captured a
bat only an average of 1.8 times; a very narrow window
through which to examine its movements. Radio tracking and
capture of bats with known day roosts showed average
movements of 1-4 km between day roost and feeding site.
Mean distances between captures show no correlation with sex
or age. Proportionately, records of movements by juveniles
were much more frequent than expected and records of adults
are about the same or a little less than expected, perhaps
reflecting the relative difficulty in recapturing older adults. The
longest distance we recorded between captures was about 6 km
for three individuals. However, these were not single-night
movements; therefore, these distances may represent dispersion
instead of actual foraging distances.
Artibeus jamaicensis often visit more than one tree in an
evening. We recaptured one individual at a fruiting tree 1.2 km
away from another tree where she had been captured earlier the
same evening. Recapture rates were only 2% for bats captured
more than once at the same tree on successive nights, and
similarly low for bats recaptured the same night at the same
station.
The number of bats at a netting station shifted during the
night, usually abruptly, suggesting that the bats are moving and
foraging in groups. These surges of activity seemed influenced
by rain, presence of ripe fruit, and phase of the moon. Clearly,
bats were least active in the week following the first quarter of
the moon (most light early in the evening), and most active in
the week following the new moon.
8. Roosting Behavior
Douglas W. Morrison and Charles O. Handley, Jr.
In this section we present a synthesis of our mark-recapture,
radio-tracking, and night-viewing-scope observations pertinent
to day roosts of Artibeus jamaicensis on Barro Colorado Island
(BCI). For comparison, we have included data on other species
of bats where appropriate. We present a similar synthesis of
observations on night roosts as part of the discussion in Section
9, Foraging Behavior.
Mark-recapture and radio-tracking techniques have inherent
strengths and weaknesses. With radio-tagging, the behavior of
individuals can be intensely monitored for days or weeks.
However, sample sizes tend to be small and there is no
independent way to measure how much the behavior of an
individual has been altered by the transmitter. In contrast,
long-term netting studies can generate huge samples, but the
data are sometimes difficult to interpret.
Taken together, the two techniques complement each other
in important ways. Questions provoked by radio-tracking
observations can provide a framework around which to analyze
mark-recapture data and netting data provide independent
confirmation that the behavior of radio-tagged individuals is
typical of the population as a whole. Using the two techniques
in concert has increased our confidence in the accuracy of the
picture that has emerged.
Bats show diverse roosting behaviors, often using different
kinds of roosts for different periods of their daily and annual
cycles (Kunz, 1982). Day roosts offer protection from predators
and the elements and are generally used for extended periods.
In contrast, night roosts may be less protected, temporary sites
chosen for their proximity to food sources. Individual bats also
may change roosts on a seasonal basis, with certain types of
roosts favored for mating, rearing young, or other activities.
Day-roosting Sites
A. jamaicensis apparently is opportunistic in its selection of
day-roosting sites. Where caves are available, it roosts in large
groups (Dalquest, 1953; Kunz, 1982; Tuttle, 1968). In forested
Douglas W. Morrison, Department of Zoology and Physiology,
Rutgers University, 195 University Ave., Newark, NJ. 07102.
Charles O. Handley, Jr., National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560.
habitats, the largest groups roost by day in tree hollows, while
smaller groups and individuals are found in foliage (Morrison,
1979). In the moist tropical forest of BCI, we located 25 day
roosts used by 18 radio-tagged A. jamaicensis. Sixteen were in
foliage and nine in tree hollows.
DAY ROOSTS IN FOLIAGE.?Foliage roosts were used
primarily by males. Seven radio-tagged males made transient
use of a variety of sites in the foliage, typically occupying a site
for 3-5 days (range 1-13 days) before moving to another
foliage site 100 m or farther away. In contrast, females
normally roosted in tree hollows and rarely used foliage sites.
Of 11 radio-tagged females, two roosted in foliage but only
after being captured and radio-tagged as they emerged from
their day roosts in tree hollows.
The kinds of foliage roosts used by A. jamaicensis (a 45 g
bat) are typical of those used by canopy-foraging fruit bats
(Goodwin and Greenhall, 1961) and were indistinguishable
from those used by A. lituratus (70 g) and Vampyrodes
caraccioli (36 g) on BCI (Morrison, 1979, 1980a). Foliage
roosts used by radio-tagged A. jamaicensis on BCI included
shelters under a long, arching frond of a palm, Oenocarpus
panamanus; under an "umbrella" formed by a single, wilted
leaf of a broadleaf epiphyte; in the crown of a spiny black palm,
Astrocaryum standleyanum; and in a shallow shelter formed by
the forest canopy.
Radio-tagged V. caraccioli (nine sightings) invariably
roosted in groups of three or four adults, 7-12 m above the
ground, under the umbrella-like crowns of understory trees
(12-20 cm Diameter at Breast Height (DBH)). The day roosts
of radio-tagged A. lituratus (26 sightings) were more variable,
from 2.7-28 m above the ground in a variety of situations, such
as under broken or crossed fronds of Oenocarpus panamanus,
in vine-tangled crowns of subcanopy trees, in cavelike recesses
on the underside of the crowns of canopy-height trees, and in
branches overhanging the water along the lakeshore.
As variable as these roosts might seem, all had two important
features in common: they were difficult to see from the ground
and they had unstable supporting structures. Despite their open
appearance, foliage roosts may be almost as effective as tree
hollows for reducing the exposure of adult bats to predation and
rain. The dense leaf cover forming the roof of these recesses is
131
132 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
waterproof and provides heavy shade. Contrary to our initial
expectations, the availability of the dark recesses these bats
prefer as day roosts may be limited, and new ones may be
difficult to find. To find a radio-tagged bat often required
searching through the foliage for hours from every possible
angle with the aid of binoculars aimed at the source of the radio
signal. When finally located, the bat was always in the darkest
of the myriad recesses overhead.
Foliage roosts would probably frustrate any attack by an
aerial predator. A terrestrial predator, even if it did see a
roosting group from the ground, would almost certainly vibrate
the highly flexible branches of these roosts and be detected
long before it could reach the group. Some arboreal predators,
such as snakes, may be stealthy enough to make their way
across the shaky fronds and branches of foliage roosts without
being detected. We observed a large green snake (Leptophis
ahaetulla) ascending along the rib of an arching frond of
Oenocarpus panamanus without obvious disturbance to the
frond. This snake probably eats lizards and frogs (A.S. Rand,
pers. comm.), but might take small bats. On the other hand,
fronds and branches sagged under the weight of a 3-m-long rat
snake, Spilotes pullatus, a known predator of bats.
Changing their roosts almost daily might make foliage-
roosting A. jamaicensis, A. lituratus, and V. caraccioli more
difficult to find. The hypothesis that day-roosts are changed to
sites closer to the fruiting trees in current use was not supported
by our observations (Morrison, 1980a). Increasing the distance
between consecutively used sites should decrease the risk from
predators attracted to an earlier site. However, foliage-roosting
bats do not range freely, but rather remain faithful to a
particular ridge or shoreline (Morrison, 1980a). Searching in a
familiar area may significantly reduce the cost of finding a new
roosting site.
DAY ROOSTS IN TREE HOLLOWS.?Naturally occurring
hollows in trees provide shelters that are more permanent.
Access to the hollows used by radio-tagged A. jamaicensis on
BCI was invariably through a single small hole or slit, about 6
cm wide, and 2-15 m above the ground. The hollows typically
were long cylinders, 12-25 cm internal diameter, extending
1.5-2.0 m above the entrance hole.
Judged by the size and location of the entrances, hole roosts
should give better protection from predators than foliage roosts,
but only if their entrance holes are neither too close to the
ground nor accessible from nearby branches. We observed
prcdation by a snake on a day-roosting group of A. jamaicensis
in the hollow trunk of a 1.1-m-DBH fig tree (Ficus yoponensis)
east of Donato 2. The entrance of the roost, 13 m above the
ground, had probably been inaccessible to snakes for many
years, until the crown of a nearby sapling (4 cm DBH) grew up
to within 0.5 m of it. On a July 1979 afternoon, during a routine
check of the roost, we watched a 1.7-m-long yellow-and-black
snake (believed to be a rat snake, Spilotes pullatus) passing
from the roost entrance into the crown of the sapling. The
departing snake had five delta-shaped bulges along its length.
Unfortunately, the belief that the bulges were bats could not be
confirmed because the snake never came lower than 12 m
above the ground before it disappeared in the subcanopy.
Individual A. jamaicensis apparently are aware of the
location of several holes suitable for roosts, but favor a
particular hole for extended periods. Eight of 11 radio-tagged
females used the same hollow or pair of hollows for the 4-22
day life of their transmitters (Morrison, 1979). The male and
four of six females trapped at a roost near Barbour-Lathrop 1
were still in residence when the roost was netted again three
months later. The movement of roosting females between tree
hollows was not completely random. For example, a female
that usually roosted near Barbour-Lathrop 1 twice used a
second hollow 100 m away. This same pair of hollows was
used by a second female two months later. Similarly, a female
that favored a hollow near Wheeler 3 also roosted in a
Quararibea asterolepis 300 m away. Three months later
another female, captured as she left the Wheeler 3 hollow, took
up residence in the Quararibea. These observations are more
likely a reflection of a shortage of preferred roosting holes than
a reflection of cohesiveness within female groups. Female
roostmates showed no cohesiveness when foraging (see
Section 9, Foraging Behavior). Further, the few females that
temporarily abandoned their tree hollows after being netted
there typically went to different alternative sites.
DAY ROOSTS IN MAN-MADE STRUCTURES.?Groups of
day-roosting A. jamaicensis were found inside the hollow
pyramidal concrete markers used as navigational aids by ships
transiting the Panama Canal. Each marker stands 7.6 m high at
the peak, is 1.5 m on each side, is open at the bottom, and
resembles a hollow pyramid on long stilts. Two such markers,
one on Buena Vista Island and the other near Palenguilla Point
(= Pefla Blanca), have been occupied by A. jamaicensis for
many years. Each of these roosts was censused ten times over
a three-year period beginning in October 1977. Of 83 adult
females trapped in these roosts at least once, 44 (53%) were
recaptured in the same roost 1-6 times. The average interval
between first and last capture was 14 ? 9 months, with 14
females in residence for over two years.
The recapture records from the Buena Vista and Pefla Blanca
markers provide a good estimate of long-term fidelity, despite
the artificial nature of the roosts themselves and disturbance by
Bat Project personnel. Actually, the average tenure of females
may be longer at hole roosts that are not so frequently
disturbed. The number of A. jamaicensis roosting in the two
markers declined steadily over the study period, probably due
to the disturbance of repeated capture. At Buena Vista, the
number of adult females went from 20-30 in 1977 to 10-15 in
1978 and 1979. By the end of 1980, only four adult females
remained, three of which were first-time captures. At Pefla
Blanca, adult females declined from 10-30 in 1977 to 10-15
in 1978 and 1979. By the end of 1980, the only two bats in the
roost were subadult females, both first-time captures.
EXPERIMENTS WITH "ARTIFICIAL" TREE HOLLOWS.?
NUMBER 511 133
Walking through a tropical forest, one can get the impression
that holes in the trunks of trees are almost as numerous as
foliage umbrellas. However, closer inspection reveals that these
holes usually open into cavities too shallow for even one A.
jamaicensis, much less a group, and many of the larger cavities
either extend down from the entrance hole (the preferred
direction is up), have an entrance hole that is too large (wider
than 6 cm), or have more than one entrance hole.
We suspected that the availability of suitable tree hollows
might be a factor limiting the population of Artibeus
jamaicensis on BCI. Finding A. jamaicensis roosting inside
concrete pyramids encouraged us to put up artificial tree
hollows to determine whether the demand for preferred roost
holes was greater than the supply and what the pattern of
colonization of new roost holes might be. From balsa trees
(Ochroma pyramidale) that we felled on Delesseps Island, a
regularly cleared area adjacent to a dangerous bend in the
Canal, we constructed 40 artificial tree hollows. The trees were
cut into 2 m lengths, 0.35 to 0.45 m in diameter, sawed in half
lengthwise and hollowed out with an ax. Internal cavities
approximated the "ideal" hole roost; 15 cm in diameter and
extending 1.1 m above a 6 cm x 40 cm entrance hole. To
facilitate inspection of roost contents with a flashlight and
mirror, a small trap door was cut in the bottom of the back half.
During July 1978, we placed the bat houses all over BCI in
habitats structurally similar to those of known hole roosts. The
hollows were lashed high enough on understory trees for the
entrance holes to be at least 1.7 m above the ground. Sixteen
roosts were placed within 800 m of the laboratory clearing,
eight within 500 m of the Tower Clearing in the center of BCI,
and four each along Miller Ridge, Chapman End, Drayton End,
and Armour End. In an attempt to make some of the new roosts
more conspicuous, ripe figs, banana, and A. jamaicensis feces
were placed inside the entrances of eight of the roosts near the
lab clearing.
We hoped that regular inspection of the roosts would reveal
some pattern in the colonization of the newly available tree
hollows and shed light on the dynamics of harem formation. Do
females aggregate at a tree hollow first, with a male appending
himself later? Or is the roost first discovered and used by a male
who then "recruits" females?
These questions remain unanswered. The hollows were a
disappointing failure. Although used by a variety of inverte-
brates and a few vertebrates, none was ever found to have been
used by bats. A thorough census in July 1979, after the hollows
had been in place for a year, revealed the most common
occupants to be termites (16 hollows), crickets (13), spiders
(11), and ants (6). Other inhabitants were whip scorpions (3),
earwigs (3), roaches (2), and geckos (2). A few contained
mammalian (2) and avian (1) nesting material. Two hollows
were completely empty. All the hollows were taken down and
destroyed in January 1980. Unfortunately, negative data cannot
be used to argue either for or against a shortage of preferred
roost hollows.
Composition of Day-roosting Groups
GROUPS IN FOLIAGE.?A. jamaicensis has been reported
roosting in large groups containing both sexes in foliage in
Trinidad (Goodwin and Greenhall, 1961) and Brazil (Jimbo
and Schwassmann, 1967). On BCI, groups of A. jamaicensis
roosting in foliage were small (1-3 individuals) and primarily
male (Morrison, 1979, table 1). Five of eight foliage roosts
were occupied by solitary adult males and another by two adult
males. The only adult females found roosting in foliage were
two that had been radio-tagged when they emerged from hole
roosts. They used foliage roosts for only two to five days before
returning to a hole roost.
GROUPS IN TREE HOLLOWS.?Hole roosts were used by
groups of adult females, their nursing young, and a single adult
male. Nine of 11 radio-tagged females used hole roosts
exclusively. The two exceptions had been captured at hole
roosts, subsequently used foliage roosts, but returned to hole
roosting a few days later.
The composition of hole-roosting groups was determined by
capturing the occupants in a "laundry-chute" trap as they
emerged in the evening. Each of six hole roosts censused this
way contained only one adult male, 3-14 adult females, and
0-6 juveniles (Morrison, 1979; Morrison and Morrison, 1981).
GROUPS IN MAN-MADE STRUCTURES.?The pattern of sexual
segregation at day roosts suggests that A. jamaicensis has a
harem mating system. This hypothesis is supported by the
long-term records of A. jamaicensis roosting inside the
navigation markers at Buena Vista and Pefla Blanca. In 18 of 20
capture episodes when adult females were present in the roosts,
only one adult male was captured or some bats escaped (among
which there might have been an adult male). We never captured
more than one adult male in a roost.
Of 46 A. jamaicensis captured as adults at the Bucna Vista
marker, only three were males. The first male was captured
three times over a 17-month period, first in December 1977 and
last in April 1980. The second was captured at the marker once,
in November 1979, after it had been marked as a subadult at
Snyder-Molino 2 on BCI in December 1977. A third was
captured in March 1980. At no time was there more than one
adult male at the roost This capture sequence suggests that the
second male had replaced the first as the harem male at Buena
Vista and was himself replaced a few months later.
Displaced harem males may be able to regain their former
position. Of 42 A. jamaicensis captured as adults at Pcfia
Blanca, four were males but no more than one was found at a
time. The first male was captured only once, in October 1977.
The second male was captured three times between April and
July 1978. The third male was captured in December 1978 and
the fourth in April 1979. The second male reappeared as the
only male present in November 1979.
Many adult females showed long-term fidelity to marker
roosts that extended far beyond the tenure of any of the harem
males. This suggests that females are attracted by the roost site
134 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
rather than by a particular male.
Juvenile females do not stay to become members of their
mother's harem. Of 31 females captured as juveniles at Buena
Vista and Pefia Blanca, only one was ever recaptured at either
(Pefla Blanca) as an adult. Instead, females leave their natal
roosting groups and join other harems as subadults. Of 21
females present at the two marker roosts as subadults, seven
(33%) were recaptured there as adults. The harems of A.
jamaicensis contain adult females of all ages, suggesting that
subadult females join established harems. In contrast, harems
of the greater spear-nosed bat, Phyllostomus hastatus, are
formed from a single generation of subadult females
(McCracken and Bradbury, 1977). Young females of the
short-tailed fruit bat, Carollia perspicillata, are more likely to
disperse away from their natal roosts than are young males, but
even so, 42% remain in the natal roost. Those roosts, however,
tend to be larger colonies in caves or hollow trees and contain
more than one harem (Fleming, 1988).
Males also leave their natal roosting groups by the time they
are subadults. None of the 21 males marked as juveniles at
Buena Vista and Pefla Blanca was ever captured again at these
roosts. The single male marked at Pefia Blanca as a subadult
was never recaptured.
Male Defense of Tree Hollows
The sexual segregation apparent at day roosts suggests that
males gain harems by defending hole roosts used by females.
This hypothesis is supported by Morrison and Morrison's
(1981) observations on the nocturnal interactions of harem
group members, monitored with an infrared viewing device in
conjunction with the radio-telemetry of individuals.
During the breeding season of June-July 1979, a tripod-
mounted, 1.5 power night-viewing device (Javelin 221) fitted
with an infrared light source was used on six nights to observe
the activity around two roost hollows. Transmitters were fitted
to each harem male and three and four of the three and 14
females in their respective harems. The harem male at a third
hole roost was also radio-tagged.
The transmitters enabled us to monitor the foraging activities
of individuals on 27 10-hour nights and to identify individuals
within the field of view of the night-viewing device. In
addition, because the relative intensities of the transmitter
pulses became distinctively modulated whenever the bats were
flying, flying times could be measured even when the bats were
not in sight.
Continuous radio contact was maintained on the three harem
males during 12 10-hour nights. All three harem males spent
over 90% of the night within 50-100 m of their respective
roost hollows. Unlike the females, who carried fruits only
25-200 m from the fruit tree to a night roost before eating
them, harem males brought each fruit back to the day roost
area. On several nights this meant the male was making feeding
passes of over 1.5 km on each roundtrip.
The foraging activities of the two males with radio-tagged
harems were closely correlated with those of their females. The
male was invariably the first out of the roost at dusk. He began
making feeding passes before most of his harem had left the
roost. Each male suspended feeding passes as soon as the first
female returned to suckle the juvenile she had left behind inside
the hollow. Females remained inside the hollow for 1-4.5
hours, depending on the phase of the moon. Both sexes
minimized flying in bright moonlight, probably to reduce the
risk of predation from visually orienting owls and opossums
(Morrison, 1978a). During these periods of inactivity, the
harem male stayed outside the roost, but did not resume feeding
passes until his females began to leave again for a second bout
of feeding. The harem male was always the last to reenter the
roost at dawn.
Harem males did an extraordinary amount of flying in the
immediate vicinity of their day-roost trees. While their females
were leaving the roost, the male preceded each of his feeding
passes with 1-4 minutes of local flying, during which he
crossed in front of the roost entrance one to five times,
occasionally hovering there for less than a second. In contrast,
when all his females were out foraging, most local flying was
done away from the roost entrance out of view of the
night-viewing scope.
Local flying probably keeps the nearby area free of potential
intruders. On two occasions the harem male chased away an
unidentified bat that repeatedly tried to enter the roost. The
unidentified bats may have been rival adult males or they may
have been young of the previous generation that were no longer
allowed to roost with their mothers. On the two nights when we
were trapping emerging harem members for radio-tagging, we
also netted two adult males and seven juveniles trying to enter
the roost.
Local flying by the harem male might also serve to advertise
the roost to females. During one predawn return, the harem
male was seen closely following (escorting?) five of his 14
females as they approached the roost entrance, circling back to
inspect the entrance after each female had entered. The
frequency and duration of local flying bouts increased during
both periods of the night when females were returning. In the
absence of bright moonlight, harem males were typically in
flight for 60 minutes of the final 90 minutes before dawn.
These observations provide additional support for the
hypothesis that A. jamaicensis males maintain harems by
defending roost holes. Although it would not seem feasible to
defend more than one female at a time when they are foraging
away from the roost, the defense of a roost hollow could
significantly increase the harem male's unimpeded access to
females in postpartum estrus. In the 18 g frugivorous
short-tailed fruit bat (Carollia perspicillata), males defend
roosting sites both in hollow trees and within the confines of
larger colonies roosting in caves (Fleming, 1988).
In two other species of Neotropical bats known to have
harems, males have evolved other strategies for harem
NUMBER 511 135
maintenance. In the 8 g insectivorous white-lined bat (Saccop-
teryx bilineata), males gain harems by defending prime feeding
territories (Bradbury and Vehrencamp, 1977a). In the 115 g
omnivorous greater spear-nosed bat (Phyllostomus hastatus),
males defend females clustered on cave ceilings (McCracken
and Bradbury, 1977). These behaviors are consistent with the
theory that harem mating systems evolve only where it is
feasible for one male either to defend a group of females
directly or to defend some limited resource used by more than
one female (Emlen and Oring, 1977).
Summary
Data from 18 radio-tagged A. jamaicensis yielded informa-
tion on 25 day roosts on Barro Colorado Island. Day roosts in
foliage are more commonly used by males than females, and
the bats typically change roosts every three to five days.
Foliage roosts occur in a variety of species of plants, but all are
difficult to see, have unstable support, and yet provide good
protection from rain and predators. These roosts probably are
used primarily by bachelor males, either singly or in small
groups.
Day roosts in tree hollows provide more permanent shelter
and probably better protection from predators. Tree holes are
occupied by harems and are defended by males. Each of six
hole roosts, censused by capturing all occupants, contained
3-14 adult females, 0-6 young, and a single adult male.
Females favor a particular hole for extended periods. Harem
males spend over 90% of each night within 50-100 m of their
hollows. Even when females are not present, the male carries
individual fruits back to the hollow to eat. Harem males do an
extraordinary amount of flying near the hole roost, chasing
away intruders and escorting returning females.
Two man-made navigational markers housed harems of bats
for extended periods of time. These roosts never contained
more than one adult male. Adult females frequently outlasted
harem males at these sites, suggesting that females are faithful
to the roost site rather than to the male. All juvenile males leave
their natal roosts by the time they are subadults. Most juvenile
females also leave their natal roosts and join other harems as
subadults.
In an effort to determine how new harems are established, we
constructed artificial tree hole roosts from pieces of tree trunk.
These artificial roosts failed to attract any bats during the
course of a one-year trial.

9. Foraging Behavior
Charles O. Handley, Jr., and Douglas W. Morrison
Enough is known about the foraging behavior of Artibeus
jamaicensis to permit a quantitative description of its daily
routine and energy budget (Morrison, 1978d; Section 2,
Physiology). However, many questions remain, especially
concerning the social aspects of foraging. Here we present a
more qualitative, at times speculative, discussion of behaviors
related to foraging, based on our radio-telemetry and mark-
recapture studies of A. jamaicensis on Barro Colorado Island
(BCI).
The Basic Feeding Pattern
From radio-telemetry of 32 individuals we know that an A.
jamaicensis typically leaves the day roost 0.5 hours after sunset
and flies directly to one of the fruit trees visited on a previous
nighL Individuals may return to the same tree for up to eight
consecutive nights (4.3 ? 1.8, n = 27 trees). A bat does not roost
in the fruiting tree to eat, but instead carries the fruit to a
feeding roost 25-200 m away. Small bites of fruit are crushed,
sucked dry, and dropped as pellets ("bat chop") under the roost.
From its feeding roost, the bat makes numerous passes to the
fruiting tree, returning with a fruit carried in its mouth each
time. At 0.5 hours before sunrise the bats return to their day
roosts.
The basic feeding pattern is affected by the phase of the
moon (Morrison, 1978a). On "dark moon" nights (one week
either side of the new moon) A. jamaicensis is active from dusk
to dawn and visits as many as five separate feeding areas (3.0
? 1.5, n = 14 nights). On "bright moon" nights (one week either
side of the full moon) the bats interrupt foraging to return to
their day roosts for one to seven hours when the moon is nearest
its zenith. On these nights, the bats usually visit no more than
two feeding areas (2.1 ? 0.7, n = 23 nights), with the more
distant one visited either before moonrise or after moonset.
"Lunar phobia" (Morrison, 1978a) and the use of feeding
roosts probably reduce exposure to predation. Bright moonlight
Charles O. Handley, Jr., National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560.
Douglas W. Morrison, Department of Zoology and Physiology,
Rutgers University, 195 University Ave., Newark, NJ. 07102.
would make a bat hovering to select a fruit more conspicuous
to visually-orienting predators such as owls and opossums.
Anecdotal evidence suggests that potential predators of bats are
attracted to fruiting trees. Judging from the number of
vocalizations heard, there seem to be more owls around trees
with ripe fruit than in other parts of the forest Furthermore,
opossums (e.g., Didelphis marsupialis) are often seen in the
branches of fig trees containing ripe fruit, and we once saw a
gray four-eyed opossum (Philander opossum) almost capture a
bat that had chanced to roost nearby. This helps explain why A.
jamaicensis does not hang in fruit trees to feed.
Lunar phobia is present, to a lesser extent, in A. lituratus and
Vampyrodes caraccioli, two other canopy fruit bats of BCI
(Morrison, 1980a). Aspects of lunar phobia that we observed in
these species may apply to A. jamaicensis as well. Perhaps
because their day roosts are in foliage rather than in tree
hollows, radio-tagged A. lituratus and V. caraccioli did not
return to them during bright moonlight, even when the day
roost was relatively close (within 350 m) to the feeding area.
However, total flying activity was reduced significantly on
bright moonlit nights.
To simplify studying activity patterns of bats we divided the
night into 15-minute intervals. On bright moon nights, A.
lituratus did not fly in 55% of the intervals, in contrast to flying
in 80% on dark moon nights. V. caraccioli showed a similar
pattern, sometimes remaining inactive (not flying) for periods
of up to four hours. Although feeding passes were suspended or
greatly reduced in moonlight, both species flew between
feeding areas and conducted prolonged search flights even in
the brightest moonlight. These behaviors suggest that the risk
of predation is greatest near fruiting trees.
Various workers (Crespo et al., 1972; Schmidt et al., 1971;
Tamsitt and Valdivieso, 1961; Villa-R, 1966; Wimsatt, 1969)
have reported catching fewer foraging bats (Desmodus rotun-
dus, A. lituratus, Phyllostomus discolor, and Glossophaga
soricina) in their nets during periods of moonlight. Eckert
(1974) painstakingly demonstrated the inhibitory effect of
moonlight on A. lituratus and P. hastatus in captivity and
Haussler and Eckert (1978) confirmed the effect on P. discolor
with simulation experiments. Several African insectivorous
microchiropterans show the same effect as evidenced by bat
137
138 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
detector recordings of activity (Fenton, Boyle et al., 1977).
Eckert (1982) argued persuasively that all such effects are
adaptations for the avoidance of visually orienting predators.
Longer-term Foraging Patterns
Patterns of fruit tree use were most apparent on bright
moonlit nights because flying was limited and feeding passes
seemed especially regimented. Occasionally on such nights, a
radio-tagged A. jamaicensis made what appeared to be a
feeding pass in the wrong direction. In some cases, these flights
were simply feeding passes to another fruiting tree, demonstrat-
ing that bats sometimes use a single night roost while feeding
on more than one tree. Or, if these were nonfeeding passes they
may have been reconnaissance flights to gain information
about future feeding sites.
Although bats returned to feed on the same fruit tree for as
many as eight consecutive nights, they discontinued feeding
visits when the density of the figs declined to less than one or
two per square meter (n = 6), unless a fig tree was less than 150
m from the day roost. In switching fruit trees, a bat typically
made no more than the first feeding pass of the night to the
previously used tree and then immediately, without search
flying, switched its feeding roost or feeding passes to a new
tree. In 11 instances this shift was to an area that the bat had
visited from 1-8 (4.2 ? 2.2) nights previously. In five of these
11 cases, the shift was to a fig tree that had almost certainly
been the object of earlier reconnaissance flights.
Flying by radio-tagged A. jamaicensis during the bright half
of the lunar month was reduced to the minimum length of time
required to get to a feeding roost (usually from one to five
minutes). Even on moonless nights, the bats often made only
short flights and spent most of their time hanging at the feeding
roosts. Occasionally, however, bouts of sustained flying that
lasted 10-45 minutes were recorded. Six of 40 all-night
tracking sessions contained at least one such period of
prolonged flying. All but one of those longer flights occurred
during the dark half of the lunar month. The one exception
occurred in the evening before a late (2345 hours) moonrise.
Prolonged flights began either from night feeding roosts (n =
3) or upon emergence at dusk from day roosts (jn = 3). The area
covered by these flights could only be approximated, as it was
not possible to triangulate the bats' constantly changing
position. Usually the flying was confined to the watershed in
which it began (n = 4), but once it shifted into an adjacent
watershed and another time into a nonadjacent watershed.
These long search flights undoubtedly increase the chances of
encountering newly fruiting trees and might have been initiated
for that purpose.
Feeding Roosts
Triangulation by radio of foraging A. jamaicensis suggests
that feeding roosts usually are in one or a few favored trees,
within a 0.25 to 0.5 ha area, 25 to 200 m from a fruiting tree.
Morrison (1975) was able to pinpoint and confirm, by on-site
inspection, two feeding roosts used by his radio-tagged A.
jamaicensis. One was in the crown of a 13-m-tall, spiny black
palm (Astrocaryum standleyanum). The other was about 3 m
above the ground under the long, arching frond of an
Oenocarpus panamanus. Both sites could have been selected
for their reduced accessibility to terrestrial predators (see
Section 8, Roosting Behavior).
After Alfred Gardner discovered that bats drop pellets of
chewed pulp when feeding on figs, Bat Project personnel
routinely used accumulations of pellets to recognize sites used
as feeding roosts. Depending on the height from which they are
dropped, the pellets may be in small piles, distinct clusters, or
broadly dispersed. The area covered can be quite extensive,
sometimes exceeding 100 m2. These feeding roosts are often
located along ridges above fruiting trees, but may be found
elsewhere, especially where young palms or subcanopy trees
are numerous. The single common feature is an open
understory that does not restrict flight. This may explain why
we have found so many feeding roosts along or adjacent to
trails, which also function as open flight paths for bats.
Radio-tagged A. jamaicensis were relatively faithful to
feeding roosts. Invariably the same feeding roost area was used
night after night for as long as a bat fed from the same fruit tree
(n = 14 fruiting trees). Four radio-tagged bats made foraging
passes from the same feeding roost to two simultaneously
fruiting trees 35-220 m apart, and two bats used the same
feeding roost areas when they returned after three and eight
nights, respectively, to get fruit from another tree in the
neighborhood.
There are several possible, but untested, explanations for this
apparent fidelity to feeding roost areas. It might simply be the
result of the patchy distribution of vegetation preferred for
feeding roosts. Or it might be that A. jamaicensis is a creature
of habit, preferring to use familiar sites along well-known flight
paths. The latter hypothesis is supported by our observation
that radio-tagged A. jamaicensis frequently did not use (or
failed to find) a fig tree producing ripe fruit close to their day
roosts. Instead they commuted two to three times farther to
another tree. This suggests that many fruiting trees are found
because they stand along familiar foraging routes.
Feeding roosts may have other functions not related to
feeding. For example, if they are closer to a fruiting tree than
the day roost, they may serve as convenient havens during
bright moonlight. This at least seems to be the case with A.
lituratus and V. caraccioli, two fruit bats that have day roosts in
foliage (Morrison, 1980a). Feeding roosts also may be sites for
social interaction. Adult bachelor males may try to copulate
with females at feeding roosts away from the day roost and its
defending harem male because they probably lack other access
to females (Morrison and Morrison, 1981). However, females
may be less receptive to males encountered outside the
day-roost hollow if competition for hollows selects for males
NUMBER 511 139
who sire stronger, more aggressive, or otherwise fitter young.
Also, day roosts are probably safer sites for copulating bats
than are night roosts.
Group Foraging
Feeding roosts might be "information centers" for food
finding (sensu Ward and Zahavi, 1973). In theory, A.
jamaicensis is a likely candidate for group foraging information
sharing. A prerequisite for the evolution of information centers
is that food be found in short-lived, locally superabundant
patches. This sort of food distribution means that users must
continually find new food patches. However, because the
patches contain so much food (and for so short a time), nothing
is gained by trying to conceal or defend a food patch once it is
found. Fig trees fit this description. A single fig tree on BCI
may bear 40,000 figs, of which a single A. jamaicensis would
likely carry away no more than 100 (Morrison, 1978d) before
the fruits were gone or spoiled.
A second characteristic that makes A. jamaicensis a potential
user of information centers is that foraging bats aggregate at
night (feeding) roosts. A night roost may be occupied by
dozens, if not hundreds, of bats, and they may be making
feeding passes to several different fruiting trees.
A simple mechanism for information exchange is plausible.
If an A. jamaicensis, which has been successful in finding a fig
tree, returns to its feeding roost with a fig or the odor of figs,
any roost mates who had been unsuccessful in finding food
could follow the successful bat out on its next feeding flight.
The information sharing would not need to be intentional, but
the information would greatly benefit the unsuccessful bat and
would not significantly deplete the food at the tree for the
successful bat. In a group that remained together over a period
of time, it is possible that tonight's successful bat could be
tomorrow night's unsuccessful bat, and vice versa, so all would
gain over the long term. Note also in this context the probability
of food finding reconnaissance flights initiated in advance of
need.
Despite the theoretical potential, it is still unknown whether
A. jamaicensis on BCI forages in cohesive groups. Certainly
this bat does forage in groups, as the nightly ebb and flow of
bats at a fruit tree demonstrates (see Section 7, Movements).
However, whether the flocks that swirl about a fruit tree stay
together for hours, all night, several nights, or for long periods
of time is unknown.
Morrison and Morrison (1981) tracked a group of three and
another of four radio-tagged female A. jamaicensis from two
different harems for eight complete nights and found no
evidence of cohesiveness of harem members away from the day
roost. These females left and reentered their day roost hole
individually. Because emergences were typically more than a
minute apart, each female emerged after the previous one had
disappeared from the day roost area. On three of the eight
nights, three of four females did visit the same ripe-fruit-
bearing Ficus insipida in the course of the night, but they
moved between fruit trees independently and did not roost
anywhere near each other while feeding. This radio-tracking
study suggests that harem females do not forage in groups, at
least not during the circumstances operant when our observa-
tions were made.
Nevertheless, it is still possible that other sex and age classes
forage in groups, or that A. jamaicensis forage together in
habitats where fruiting trees are not as abundant and easy to
find as they are on BCI. In Mexico and Costa Rica, for
example, clumped mist-netting capture times have been
interpreted to mean that the A. jamaicensis there forage in
groups (Dalquest, 1953; Heithaus et al., 1975). Group foraging
has been reported in flower-feeding bats in Brazil (Sazima and
Sazima, 1977) and Arizona (Howell, 1979).
It should be possible to detect foraging-group associations
by analysis of the occurrence of "double recapture pairs" in the
mark-recapture data. A "double recapture pair" consists of two
bats that were captured at the same netting site on the same date
and were subsequently recaptured together at another site some
days, months, or years later. Morrison (1975) found 22 such
pairs among the 259 recaptures of 1472 A. jamaicensis he and
Bonaccorso marked over a 14-month period in 1972 and 1973.
What is the probability that this number of double recapture
pairs might occur simply as a result of chance associations in a
population of independently foraging bats? Given that two or
more recaptures are made on night n, let Pn stand for the
conditional probability that any two of these recaptures were
captured together previously (Morrison, 1975). If (n - 1) = the
number of previous capture nights, \{ = the number of bats
captured on previous capture night i, where l<i<n - 1, and y =
the total number of bats banded to night n, then
P = y fr1)
n
 SS y (y-D
The number of double recapture pairs Cj that could be expected
to occur by chance on any night n is simply Pn times the total
number of pair combinations of recaptures on night n, or Pa
times c2r, where zn is the number of recaptures on night n. The
total numer of recaptures expected to occur by chance during
the entire 14-month netting program is the sum of the P
 n. c /
values of all 60 of the 131 sampling nights in which two or
more recaptures were made. This sum was calculated and found
to equal 14.2, the number of double recapture pairs expected to
occur simply by chance. The observed value of 22 was not
significantly greater than that expected from random assort-
ment as determined by a one-tailed binomial test, P = 0.195 (the
a priori expectation for higher than random assortment,
justified the use of a one-tailed test). Thus, Morrison concluded
that A. jamaicensis does not forage in groups, at least not in
groups with memberships sufficiently constant over the long
term to be detected by this method.
However, this conclusion was based on the unrealistic
140 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
assumption that there is no mortality of marked bats. The
chance that a marked bat will die reduces the expected number
of double recapture pairs and so increases the significance level
of the observed value. To reflect this reality we used the
equation
a
~
Here it is reasonable to make s equal to 0.57, the annual
survivorship for adult A. jamaicensis (see Section 6, Population
Estimates), and for t? we use 0.32 years, the average interval
between recaptures for Morrison's (1975, table 1) data. The
expected value now drops from 14.2 to 9.9 [14.2 x (0.57)0-64].
The observed value of 22 double recapture pairs is significantly
greater than this revised expected value (one-tailed binomial
test, P < 0.05).
Unfortunately, even if these revised calculations reveal an
incidence of double recapture pairs significantly greater than
expected, we still cannot be sure that this difference is due to
the existence of foraging groups. Other factors could produce
the same result. For example, the probability of observing a
double recapture pair would be increased if independently
foraging bats frequented the same feeding area. Two bats might
frequent the same area because it is especially attractive (e.g.,
the great Lutz fig patch) or because it is near the day roosts of
both bats. The calculations of site fidelity (see Section 7,
Movements) indicate that the capture sites were not in equally
attractive areas and that individual bats were not equally likely
to be captured at all sites. Furthermore, we suspect that after the
first capture, bats tend to avoid mist nets because they are
seldom recaptured (see Section 6, Population Estimates).
Recapture pairs might be together at fruiting trees many times
before one or both are recaptured again.
These inequalities tend to increase the expected number of
double recapture pairs. Without some estimate of the magni-
tude of these biases, any test for foraging groups based on the
incidence of double recapture pairs will be inconclusive.
Thus, although clustered capture times and double recapture
pairs suggest group foraging, we lack sufficient evidence to
show that these associations are anything more than coinciden-
tal. A powerful test for group foraging could be based on direct
observation of the foraging movements of a large number of
radio-tagged bats captured together at the day roost or captured
in "clusters" while foraging. This remains to be done.
Summary
The usual pattern for an A. jamaicensis is to leave the day
roost half an hour after sunset, fly to a fruit tree, take a fruit to
a nearby feeding roost, consume it (dropping dry pellets to the
ground beneath), make several more feeding passes to the fruit
tree, then return to the day roost half an hour before sunrise. On
dark moon nights, a bat may visit as many as five feeding areas.
On nights with bright moonlight, bats visit only one or two
feeding areas, and several hours may be spent back in the day
roost during the brightest hours. Both lunar phobia and the use
of feeding roosts separate from the fruiting tree may reduce
exposure to predation.
Radio-tracking observations suggest that bats sometimes use
the same feeding roost to make feeding passes to more than one
fruiting tree. The bats also appear to make brief reconnaissance
flights to assess the condition of previously located fruit trees.
The bats spend most of their time hanging in the feeding roost
and seem to minimize feeding time even on dark moon nights.
Prolonged flights of 10-45 minutes (searching for new trees?)
were rare and occurred only in the absence of bright moonlight.
Feeding roosts tend to be groups of favored trees 25-200 m
from a fruit source, and most are located in areas of open
understory. Bats are faithful to individual feeding roosts as long
as the nearby fruiting tree remains productive. This fidelity may
result from patchy distribution of preferred roosting trees, or
may simply reflect the habitual use of a familiar area.
The bats clearly congregate at food sources, but whether
cohesive, long-term group foraging occurs is unknown.
Clustered capture times and double recapture pairs suggest
group foraging, but direct observation of the phenomenon is
lacking. Radio-tracking data on females from the same harem
show no evidence of such flocking.
Whether or not A. jamaicensis forms foraging groups, the
potential exists for an exchange of food location information
among individuals at feeding roosts. Foraging theory suggests
that feeding roosts could be information centers for finding
trees with ripe fruit (short-lived, locally superabundant food
patches), especially if the bats using a night roost are making
feeding passes to different fruiting trees.
10. Food Habits
Charles O. Handley, Jr., Alfred L. Gardner,
and Don E. Wilson
Initially, the Bat Project focused entirely on capturing and
marking bats, and little attention was given to food habits and
other aspects of natural history. Gradually it became apparent
that capture rate usually was linked to the foraging behavior of
the bats and to the location of nets in relation to food sources
and feeding roosts. Consequently, Bat Project personnel took
increasing interest in the content of the bats' feces, in evidence
and location of feeding roosts, in food items carried by bats into
nets, and in the location and phenology of fruiting trees. As a
result, capture effort became more productive in number of bats
marked and recaptured. Although our data on food habits lack
the precision of the smaller-scale studies of Bonaccorso (1979)
and Heithaus et al. (1975), they do offer insights on food
preferences, seasonality of food availability, and the foraging
habits of Artibeus jamaicensis on Barro Colorado Island (BCI).
Project personnel eventually established a protocol that
included searching for evidence of bat activity before selecting
sites as capture stations. Along the trails we watched for pellets
("bat chop") that stenodermatine bats spit out after chewing and
pressing the juice from the pulp of fruits such as Ficus insipida,
F. yoponensis, and Spondias radlkoferi. The pellets appear in
discrete piles or loose clusters on the ground when the bats drop
them from roosts low in the subcanopy, or they may be
scattered, as though broadcast, when they are dropped from the
canopy. Because the bats return again and again during the
night to the same perch, piles of pellets may represent many
fruits.
We also watched for fragments of partly eaten fruits; large
seeds such as those of Spondias mombin, S. radlkoferi, and
Dipteryx panamensis discarded by bats after they had scraped
off the pulp; cast off skins of fruit such as Quararibea
asterolepis; and trees dropping ripe fruit of kinds known to be
favored by bats. Congregations of noisy diurnal frugivores such
as monkeys (Alouatta palliata and Cebus capucinus), guans
Charles O. Handley, Jr., and Don E. Wilson, National Museum of
Natural History, Smithsonian Institution, Washington, D.C. 20560.
Alfred L. Gardner, NERC, US. Fish and Wildlife Service, National
Museum of Natural History, Washington, D.C. 20560.
(Penelope purpurascens), and parrots (Amazona spp.) often led
to the discovery of trees with ripening fruit.
We left the trails to search under certain trees (e.g.,
Oenocarpus panamanus Bailey and Gustavia superba (Hum-
boldt, Bonpland, and Kunth) (Berg) particularly favored by
bats as feeding roosts. We found that patches of these trees
associated with several fruit trees were used repeatedly by A.
jamaicensis as feeding roosts. Thus, in the course of a year, the
bats may use the same feeding roost many times. Taking this
into account, we routinely inspected known feeding roosts in
addition to walking the trails in search of new sites.
Fruits Used as Food
Our observations on fruits eaten by A. jamaicensis, mostly
late in the rainy seasons (August to November) of 1979 and
1980, are summarized here (Figure 10-1 and Table 10-1).
Ficus insipida Willdenow: Bonaccorso (1979), Fleming
(1971), Morrison (1978d), and our own observations agree that
in central Panam? F. insipida is the favorite food of A.
jamaicensis (Figure 10-1), A. lituratus, and perhaps Vampy-
rodes caraccioli, and is eaten in lesser amounts by several other
bats. Its fruit production is aseasonal, but the crop is limited in
October and from January through March (Table 10-1). Few
fruits reach maturity in August and September, two months
when F. insipida does not seem to be a significant food for bats.
Large concentrations of bats, mostly large stenodermatines,
were found near F. insipida bearing ripe fruit in March, April
(four sites), May, June, October (two sites), November (two
sites) and December. Normally the bats pick soft, fragrant, fully
mature fruit, but occasionally (as was noted on 11 January, 8
February, 21 October, and 7-9 November when few suitable F.
insipida were available) A. jamaicensis carried partly eaten
small, hard, and latex-laden unripe fruits into the nets.
Ficus yoponensis Desvaux: Similar to F. insipida in
abundance and seasonal availability on BCI (Table 10-1), the
small-fruited F. yoponensis is a favorite of smaller frugivores
such as Uroderma bilobatum, Vampyressa pusilla, V. nym-
phaea, and Vampyrops helleri and is consumed in great
141
142
Ficus inslpida
Ficus yoponensis
Ficus sp.
Ficus trlgonata
Ficus obtusifolia
Ficus costaricana
Ficus popenoel
Dlpteryx panamensis
Quararlbea asterolepis
Spondias mombin
Spondias radlkoferi
Poulsenla armata
Anacardium excelsum
Calophyllum longifolium
Cecropla sp.
Unidentified fruit pulp
Unidentified seed
Pollen on fur
JAN FEB MAR
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
APR MAY AUG SEP OCT NOV DEC
3 A
FIGURE 10-1.?Seasonal distribution of foods of Artibeus jamaicensis on BCI observed during the period
1977-1980. Squares represent seedless feces, circles represent feces with seeds, and triangles represent fruit
carried into nets. Numbers represent observations per month.
quantities by larger stenodermatines when F. insipida is scarce.
Although we caught large numbers of A. jamaicensis at fruiting
F. yoponensis, we often had the experience of netting under a
tree dropping ripe figs and finding the area devoid of bats, or of
catching A. jamaicensis carrying F. insipida from some more
distant tree. Bats with feces containing seeds of F. yoponensis
were outnumbered by about two to one by bats with feces
containing F. insipida. However, large concentrations of bats
were found at ripe F. yoponensis in May, October (two sites),
and November (three sites).
Ficus dugandii Standley: On the breezy nights of 25 and
26 October 1979, a giant F. dugandii, with a crown emerging
above the canopy near the highest point of the island, attracted
(perhaps by wind-wafted odor) large flocks of unmarked
stenodermatines, presumably from the mainland. In mist nets
beneath the tree, which was dropping many ripe fruits, we
captured only 106 A. jamaicensis, 7 A. lituratus, and 2 V.
caraccioli, while the catch of smaller stenodermatines totalled
an astonishing 265, including 138 Uroderma bilobatum, 90
Chiroderma villosum, 15 Vampyressa nymphaea, 6 V. pusilla,
1 Vampyrops helleri,! Artibeus phaeotis, 1 A. watsoni, and the
only A. hartii ever taken on BCI.
Ficus trigonata Linnaeus: The red-spotted, small-seeded
fruit of Ficus trigonata was an important food of A. jamaicensis
and C. villosum at the height of the rainy season in September
when fruit of F. insipida and F. yoponensis was scarce (Table
10-1). Many fruits of F. trigonata were carried into the nets and
its seeds were common in feces (Figure 10-1). F. trigonata also
occasionally was found in the feces of Carollia perspicillata
and Phyllostomus hastatus. Although commonly seen in
September, the lean month, the fruit of F. trigonata seemed not
to dominate the diet of any bat in that month save possibly
Chiroderma villosum. Spondias mombin and Quararibea
asterolepis were eaten more commonly. One F. trigonata was
NUMBER 511 143
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144 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
carried into a net by an A. phaeotis in March.
Ficus obtusifolia Humboldt, Bonpland, and Kunth: The
large velvet-skinned fruits of F. obtusifolia were carried into
nets occasionally by A. jamaicensis, A. lituratus, and C.
villosum. The fruits seemed to be more attractive to the smaller
frugivores such as C. villosum. We found bats concentrated at
an F. obtusifolia with ripe fruit in March.
Ficus popenoei Standley: The velvety, oblong fruits of F.
popenoei are uncommon on BCI, and we found only a few trees
with fruit. We netted near one that was dropping great
quantities of ripe fruit, and although we caught a number of
small stenodermatines of various species, the tree was ignored
by A. jamaicensis and the other larger fruit eaters.
Spondias mombin Linnaeus: An important food of bats
(Gardner, 1977), S. mombin, ripens in August and September
when fig production is low. It is found in scattered patches in
the young forest on the lower-lying areas of the island.
Apparently A. jamaicensis ingests the pulp of this fruit without
trying to extract the juice and, thus, does not make pellets.
Although S. mombin fruit seldom was carried into the nets,
those nets set nearest to trees with ripe fruit invariably caught
the most A. jamaicensis and C. perspicillata. A large
concentration of bats, mostly A. jamaicensis, was found in a
patch of S. mombin between 12 and 17 September.
Spondias radlkoferi Donnell Smith: Widespread on BCI,
but neither forming patches nor producing such great quantities
of fruit as S. mombin and Q. asterolepis, S. radlkoferi is an
important source of food for bats in the season of fig scarcity at
the height of the rains. Fruit of this tree is ripe from September
to November and is much sought by A. jamaicensis, A.
lituratus, A. phaeotis, A. watsoni, and V. caraccioli. In 1979,
ripe fruit began to fall on 19 September. Many fruits were
carried into the nets on 26 September, and by 30 September
most A. jamaicensis and A. lituratus that we captured were
eating it. A large concentration of bats was associated with a S.
radlkoferi with ripe fruit on 7 October. The last time we noted
feces containing fruit pulp of this species was on 7 November.
Seeds of S. radlkoferi with much or all of the pulp scraped off
by bats were common under feeding roosts throughout
October.
Quararibea asterolepis Pittier: The beautiful Q. asterole-
pis grows in patches, which frequently contain many individu-
als, mostly in the old forest on the elevated interior of the
island. We found it at lower elevations at Snyder-Molino 2,
Shannon 1, mouth of Barbour Creek, Standley 16, and Wheeler
26.5. When its fruit ripens in August, September, and October
it is the most abundant tree on the Plateau with fruit eaten by A.
jamaicensis. Individual trees drop large quantities of ripe fruit
over a period of two or three weeks or more. We found
concentrations of bats at Q. asterolepis with ripe fruit on three
occasions in September, and A. jamaicensis and C. perspicil-
lata frequently carried the fruit into our nets. The fibrous fruit
shell remains for weeks on the ground under feeding roosts,
persisting long after the fruiting season has passed. Q.
asterolepis and S. mombin, together with the much less
abundant F. trigonata, are the fruits of choice for A.
jamaicensis in September, and possibly in August as well,
when fruits of F. insipida and F. yoponensis are scarce or
absent. It is of interest that Q. asterolepis and S. mombin, which
fruit simultaneously and are visited by the same bats, have
complementary, nearly nonoverlapping distributions on BCI.
Both occur in patches and produce much more fruit than the
vertebrate frugivores can consume. Near fruiting Quararibea
astrolepis, A. jamaicensis usually was caught in small groups
rather than in such large concentrations as often appeared at
favored fig trees at other seasons. Some Q. asterolepis, even
when dropping quantities of fruit, almost seemed to be ignored
by bats on some nights when we netted near them.
Dipteryxpanamensis (Pittier) Record and Mell: During the
dry season when fig productivity is low, the fruit of D.
panamensis is an important food of A. jamaicensis. On BCI
Dipteryx is a widespread and abundant tree,'sometimes forming
large patches (as at Zetek 22 and east of Standley 19). Its fruit
is ripe from December to March and occasionally at other
seasons of the year (fruit was carried into a net in mid-
November). We found large concentrations of bats, principally
A. jamaicensis, at ripe D. panamensis in January 1979 and
February 1978, when numerous fruits were carried into the
nets.
Brosimum alicastrum Swartz: Robin Foster (pers. comm.)
regards bats as the principal dispersers of B. alicastrum seeds,
and Croat (1978) believed that B. alicastrum is second only to
figs in importance as a food for forest animals. We found a
large concentration of bats, including almost 100 A. jamaicen-
sis, at a Brosimum bearing ripe fruit in May. However, a large
tree raining ripe fruit in October, near the end of the fruiting
season, was attractive to kinkajous (Potosflavus) and peccaries
(Tayassu tajacu), but apparently was of little or no interest to
bats.
Anacardium excelsum Bertero and Balbis: Abundant and
widespread, and fruiting from March to May, A. excelsum is an
important food of C. perspicillata. We often caught this bat,
and A. phaeotis on one occasion, carrying the fruit of A.
excelsum. Except for one fruit carried into a net in March, we
have no evidence that A. jamaicensis eats the fruit of this
species.
Poulsenia armata Miguel: The spiny fruits of P. armata
occasionally were carried into the nets by A. phaeotis (January,
September, and October), A. watsoni (October), and once by a
A. jamaicensis (November).
Calophyllum longifolium Willdenow: In September and
October we often found the large seeds of C. longifolium under
dining roosts of A. jamaicensis, and occasionally we found
remains of pulp and skin in the feces of this bat. The pellets
from the fruit of C. longifolium dropped by A. jamaicensis and
A. lituratus seem extremely resistant to decay and persist on the
ground for several weeks. Although the large round seeds are
conspicuous, the pellets are much smaller and darker than those
NUMBER 511 145
dropped by A. jamaicensis when feeding on figs, and
consequently we often overlooked them. Fruits of C. longifo-
lium that were carried into nets by bats were offered to A.
jamaicensis, A. lituratus, and V. caraccioli temporarily held in
captivity on BCI. Both species of Artibeus ate the fruit, but V.
caraccioli did not, although it readily ate figs when those were
offered.
Cecropia spp.: Occasionally we found seeds of unidenti-
fied species of Cecropia in feces and under feeding roosts of A.
jamaicensis.
Guettarda foliacia Standley: Partly eaten fruits of G.
foliacia were found beneath feeding roosts, probably of A.
jamaicensis, in September 1979 and October 1978.
Hura crepitans Linnaeus: Numerous fleshy staminate
flower stems of Hura crepitans were carried into nets by
Phyllostomus discolor, A. jamaicensis, and A. lituratus in
November.
Unidentified Pollen: In November and December, numer-
ous bats of the species Phyllostomus hastatus, Glossophaga
commissarisi, Uroderma bilobatum, U. magnirostrum, A.
jamaicensis, and A. lituratus were stained yellow with
unidentified pollen (probably mainly from flowers of the
Bombacaceae).
Tree Selection
We know that A. jamaicensis will eat a variety of fruits, and
sometimes other foods, but most of its meals are figs. On BCI
it prefers F. insipida over all other figs, and it must be a rare
night on the island when there are no ripe fruits of this species
available. We have no idea why A. jamaicensis occasionally
chooses the fruits of Brosimum, Calophyllum, Dipteryx,
Quararibea, or Spondias over Ficus, but we have learned much
about why and when they choose a particular fig tree.
The normal massive crop of figs of each tree goes through
several stages of harvest as it ripens. First come the howler
monkeys (Alouatta palliata), which begin to eat the fruit long
before it is ripe, while the pulp is hard and the skin is still full
of latex. The monkeys are followed by the local bats from
nearby roosts. They also begin to harvest a crop before it is
fully ripe, probably selecting scattered ripe fruit, and some-
times picking unripe fruit. We have caught A. jamaicensis
carrying unripe figs, but we do not know whether they actually
eat such fruit, and if they do, whether they eat all or only part
of it. Perhaps they are sampling crops to determine the stage of
ripeness. Pellets dropped by local bats may be conspicuous
during several nights before enough of the fruit crop is ripe to
attract large groups of bats.
When the big crop finally is fully ripened, bats at the tree
may number in the hundreds or even thousands. They come in
surges, and some may stay in the vicinity all night (see Section
7, Movements and Section 9, Foraging Behavior). Groups will
return to a tree that has a big crop for three or four nights. In the
final stage of harvest, monkeys, other diurnal frugivores, and
local bats still return to the tree after its crop has been too
depleted to continue to attract large flocks of bats. Altogether,
local bats may harvest figs from a tree over a period of eight or
nine nights.
Some trees produce large crops that ripen a few figs at a time
during a prolonged period (up to 10 to 15 days) rather than
ripening abruptly as figs normally do. These trees are attractive
to local bats and nonchiropteran frugivores, but not to groups of
bats, except for brief passes.
The remnants of fig crops aborted because of lack of
pollination by fig wasps, or because of infestation with larvae
of beetles and flies, as well as the crops produced by small,
young trees, might not attract many bats. Size of the fruit crop
has an important bearing on its use by bats. Small crops may be
harvested by local bats, but usually they are not attractive to
groups. Because monkeys {Alouatta palliata) begin to harvest
a crop before bats do, they may strip a small crop before it is
ripe enough to attract bats. Local bats may help finish
harvesting a crop that is too small to attract a group. Or, a group
may make one or two feeding passes and then leave.
Radio-tracking revealed that a bat may visit three to five trees
in a night (Morrison, 1978a).
The fruits of figs are subject to destructive processes such as
infection with fungi and infestation by insects that make them
unattractive to bats. During the rainy season we often saw F.
insipida infected with a fungus manifested in fully developed
ripe fruit that have a bearded appearance while still on the tree.
As falling fruit accumulates, the ground beneath the tree
becomes carpeted with the fuzzy white fruit. Nothing eats it, in
the tree or on the ground, and eventually it rots away. Fungi, as
well as invertebrates of the litter, accelerate the breakdown of
the pellets of chewed fig pulp dropped to the ground as bats
feed. Only the most discerning eye will spot traces of these
pellets four or five days after they have been dropped.
The fruit of both F. insipida and F. yoponensis can be
infested by the larvae of flies and beetles. If the infestation is
heavy, the tree aborts part or all of its crop at about the sixth
week (about three-fourths of the way through the developmen-
tal cycle). These hard, latex-laden, and insect-riddled fruits are
eagerly eaten by monkeys (both Alouatta palliata and Cebus
capucinus), frugivorous birds, and terrestrial frugivores such as
pacas (Agouti paca), peccaries (Tayassu tajacu), and tapirs
(Tapirus bairdii). However, although they may be large and
appear to be ripe, they are not sweet, and they are ignored by
bats. Until we learned the nature of this kind of fruit-crop
abortion, we sometimes wasted effort by netting at these trees.
We were misled by the abundance of falling fruit and the
feverish activity of many frugivores into believing that bats
also would flock to the tree.
Summary
Because capture rate is clearly linked to foraging behavior,
we gathered data on fecal contents, feeding roosts, food carried
146 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
into nets, and on the location and phenology of fruiting trees.
The bats' habit of dropping small pellets of chewed fruit pulp
under favorite feeding roosts frequently dictated our choice of
netting sites. Congregations of diurnal frugivores led us to trees
with ripening fruit that would be visited at night by bats.
Certain species of trees favored as feeding roosts are used
repeatedly, especially in the vicinity of fruiting trees.
Fruit of the fig Ficus insipida is the favorite food of A.
jamaicensis as well as several other bats on BCI. Fruits of other
species of figs, including F. yoponensis, F. dugandii, F.
trigonata, and F. obtusifolia, are sometimes eaten by A.
jamaicensis, but the uncommon F. popenoei is ignored.
Spondias mombin, S. radlkoferi, and Quararibea asterolepis
are important food sources late in the rainy season when figs
are scarce. Dipteryx panamensis is used in the dry season as an
alternate food source. The fruits of Anacardium excelsum and
Poulsenia armata and the flowers of Hura crepitans occasion-
ally are eaten by A. jamaicensis.
The normal massive crop of a F. insipida is used by local
bats for several days before the entire crop is fully ripe, at which
time hundreds or even thousands of bats may visit the tree for
three or four nights until the crop is depleted. Then local bats
continue to use the tree for several nights until there is no more
fruit. Trees with small crops and trees producing crops that
ripen asynchronously over a period of a week or more are
visited by local bats but are largely ignored by groups.
11. Diet and Food Supply
Charles O. Handley, Jr., and Egbert G. Leigh, Jr.
Bonaccorso (1979) argued that food supply limits popula-
tions of bats on Barro Colorado Island (BCI). Late in the rainy
season when fruit is scarce, he found more fruit bats with empty
stomachs than he did at other times of year. About 83% of the
frugivores he netted in October and November had empty
stomachs, in contrast to 71% of those netted in March and April
when fruit was far more abundant. However, these data must be
interpreted with caution. Bonaccorso kept his data free of bias
by netting the same localities each month, without regard for
presence or absence of fruit near the netting stations. The bats
he caught with empty stomachs must have been on their way to
someplace else where there was fruit They could not endure
empty stomachs for more than a few hours without starving to
death.
Moreover, Bonaccorso (1979) observed that birth (and
breeding) of bats is timed to coincide with seasons of fruit
abundance, with one birth peak in March and April coinciding
with the fruiting peak at the onset of the rainy season and
another in July and August coinciding with the fruiting peak of
August and September (Figures 4-6 and 4-7). Few frugivorous
bats give birth between November and mid-March when fruit is
least abundant.
Bonaccorso (1979) also found that the diets of various
species of bats that forage for fruit in the canopy differed to the
extent one would expect if these animals were food limited. He
found that larger bats ate larger figs such as Ficus insipida and
F. obtusifolia, whereas smaller bats concentrated on smaller
figs such as F. popenoei and F. yoponensis. For the three larger
frugivores (Artibeus lituratus, A.jamaicensis, and Vampyrodes
caraccioli), he found that the regression of the mass Y of a fruit
carried by a bat on the mass X of its carrier was Y =
0.23X - 3.92 g (r2 = 0.46, n = 27). Presumably, smaller bats
carried fruit into the nets so rarely that he could not extend the
regression.
Reading the mass of these fruits from Bonaccorso's graph
and calculating the mean and standard deviation of the
logarithms of the mass of the fruits these bats carried, we
Charles O. Handley, Jr., National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560.
Egbert G. Leigh, Jr., Smithsonian Tropical Research Institute, Unit
0948, APO AA 34002-0948 or Apartado Box 2072, Balboa, Republic
of Panama.
derived values of 2.30 ? 0.24 (n = 6) for A. lituratus, 2.04 ?
0.33 (n = 17) for A. jamaicensis, and 1.54 ? 0.31 (n = 4) for V.
caraccioli. The standard deviations are roughly equal to the
differences between neighboring means. May and MacArthur
(1972) showed that in an idealized competitive community,
species could coexist securely if the sizes of foods eaten by the
various species differed to this extent. Excepting Artibeus
phaeotis, which eats few figs, the ratio of the mass of each
species of canopy frugivore to that of its next smaller
competitor was roughly the same as in these three species,
about 1.4 : 1 (Bonaccorso, 1979).
It is tempting to assume that the relation between the sizes of
the smaller stenodermatines and the sizes of fruit they eat is the
one Bonaccorso inferred from the few data on his largest
frugivores. Furthermore, we could conclude from the elegant
theory developed by May (1974) and May and MacArthur
(1972) on niche overlap, that the canopy frugivores coexist by
virtue of the differences Bonaccorso observed in the sizes of
fruit these bats eat
Ideally, if all sizes of figs were available at all times and were
uniformly distributed, the smaller bats would usually take the
smaller figs and the larger bats would usually take the larger
figs. However, small-fruited and large-fruited species of figs
are not uniformly distributed either in time or space, and the
bats are adaptable enough to take what is available. Of course,
in standardizing their diets, it is also necessary to take into
account the foraging behavior of these bats. The energy
expended in commuting from dining roost to fruiting tree
makes it energetically imprudent for the large bats to routinely
feed on small figs from each of which they would extract a
comparatively tiny amount of nutrients (see Section 2,
Physiology).
Fig Production
When we became concerned about the relation between food
availability and the bats' energy requirements (see Section 2,
Physiology), we began to gather information on estimates of fig
production on BCI. Each individual fig tree bears fruit to its
own rhythm (Morrison, 1978d) so that at any season some trees
are bearing ripe figs (Table 10-1). Fig production peaks early in
147
148 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
the dry season in December and January, when other fruit is
scarce, and there seems to be a lower peak at the beginning of
the rainy season. Sometime between July and November, a
month may elapse during which no more than one of the 130 fig
trees in the Lutz Watershed will produce a crop of fruit. This
low could very well be an islandwide phenomenon (Morrison,
1978d).
In the 25 ha of high second-growth forest of the Lutz Ravine,
the 49 F. insipida produced 42 full crops of fruit per year
between March 1973 and March 1975 (Morrison, 1978d) and
34 full crops of fruit per year in the 4-year period beginning 1
January 1976 (Table 10-1). The 71 F. yoponensis produced 64
full crops of fruit per year during each period.
We have two estimates of the size of a full crop of figs.
Hladik and Hladik (1969) counted 8,000 figs on a F. insipida
that had roughly 100 m2 of crown, or 80 figs per square meter
of crown. They thought the crop measured a little low.
Morrison (1978d) recorded 112 figs per square meter in a
1.3-m2 section of a crown of F. yoponensis and 113 figs per
square meter in a 3.9-m2 section of a crown of F. insipida. For
both species, the average crown area was 345 m2, so there may
be about 40,000 figs in the average full crop. The 25 ha of Lutz
Ravine, accordingly, could yield about 100,000 fruits of F.
yoponensis and about 60,000 fruits of F. insipida per hectare
per year.
Morrison (1978d) calculated average mass for F. insipida
fruits as 9 g, 81% of which was water. His average mass for F.
yoponensis was 3.5 g, again 81% water. Accordingly, we
estimated that 100 kg dry mass of F. insipida fruit and 70 kg
dry mass of F. yoponensis fruit are produced per hectare per
year in the 25 ha of Lutz Ravine. These figures are probably
representative for the other second-growth forest of the island.
The old forest has far fewer fig trees and, consequently, much
lower production of figs than does the second-growth forest in
Lutz Ravine. Older forest covers roughly half of the surface
area of BCI. Therefore, we estimate that, islandwide, fig
production is roughly 100 kg dry mass of fruit per hectare per
year.
Figs Consumed by Bats
We also wanted to know how our estimates of the
availability of figs on BCI compared with the capability of the
canopy frugivores for consuming figs and their feeding rates.
Morrison (1978d) determined that a A. jamaicensis ate an
average of seven F. insipida fruits per night (n = 7 nights). He
assumed from Bonaccorso (1975) that the fruits of F. insipida
consumed by A. jamaicensis weigh an average of 9.5 g each.
However, in December 1979 and January 1980 we found the
average fresh mass of fruits of F. insipida carried into nets by
A. jamaicensis and A. lituratus to be 6.8 g (n = 40). If a 45 g A.
jamaicensis processes seven figs with a total fresh mass of 49
g, or 9 g dry mass of fruit per night, then the estimated resident
population of 3,000 A. jamaicensis on BCI might consume an
average of 7 kg dry mass of fruit per hectare per year, and the
total population of residents and transients together, might
consume an average of 9 kg dry mass of fruit per hectare per
year. These uncritical evaluations indicate that these bats eat a
surprising amount of fruit per year.
Based on the overall data set for the Bat Project, we believe
that about one-third of the frugivorous bats that forage in the
forest canopy on BCI are A. jamaicensis, one-third are A.
lituratus, and all the other stenodermatines make up the other
third. If we assume from Bonaccorso (1979) that 65% of the
diet of A. lituratus, 76% of the diet of A. jamaicensis, 30% of
the diet of A. phaeotis, and 81% of the diet of the other
stenodermatines is figs, then these frugivores process 28 kg dry
mass of figs per hectare per year. In all, the frugivorous bats of
the canopy of the forest on BCI eat roughly 40 kg dry mass of
fruit per hectare per year when all sources are considered.
Competition and Food Limitations
Aside from bats, howler monkeys Alouatta palliata are the
primary consumers of figs. Howler monkeys on BCI eat an
average of 90 kg dry mass of food per hectare per year (Nagy
and Milton, 1979), about half of which is fruit (Hladik and
Hladik, 1969; Milton, 1978). Howler monkeys near Lutz
Ravine spend over 50% of their foraging time in fig trees eating
fruits and leaves. Troops in old forest habitats near the center of
the island spend more than 25% of their time in fig trees. In all,
they may well eat 20 kg dry mass of figs per hectare per year.
These monkeys and kinkajous (Potos flavus) are important
competitors of bats because they eat figs before the fruits are
ripe enough to attract bats and because they knock down many
figs in the process of foraging. Figs attract many other animals,
such as guans (Penelope purpurascens), toucans (Ramphastos
spp.), coatimundis (Nasua narica), and other primates such as
the night monkey (Aotus lemurinus) and the capuchin (Cebus
capucinus), but considering the year as a whole, these are
incidental competitors that depend primarily on other foods.
Despite a remarkably tight fit between numbers of bats,
consumption of figs, and supply of figs, the breeding cycle of
A. jamaicensis seems related to the abundance of fruit in
general, not to the rhythm of fig production. Fruiting of figs
peaks in December and January when few bats are being born.
To be sure, a variety of other trees composing the forest
canopy, notably Anacardium excelsum, Licania platypus,
Spondias radlkoferi, Calophyllum longifolium, Symphonia
globulifera, Brosimum alicastrum, and Poulsenia armata
produce fruits apparently designed to attract bats (Robin Foster,
pers. comm.; also see Gardner, 1977). Because all of these trees
produce green fruit that is often difficult to see, phenological
records are far from precise, but it is clear that their fruiting
rhythms will not resolve our puzzle. A few of these species fruit
when young bats are being born: Anacardium excelsum in April
and May, and Licania platypus in July and August. The others
either fruit at odd times, as does Calophyllum longifolium.
NUMBER 511 149
which may fruit in December and January and again in June
and July, and Spondias radlkoferi, which fruits in October and
November; or they fruit irregularly, perhaps several times a
year, as do Poulsenia armata and Brosimum alicastrum. From
August to October bats sometimes eat bright-colored fruits
such as Spondias mombin and Quararibea asterolepis, both of
which also attract other animals.
The breeding rhythm of frugivorous bats seems dictated by
the availability of edible fruit in general and not of fruit
preferred by bats alone. When the fruit supply is short in the
forest all over the island, animals of all kinds focus on what is
left. If this remainder is mostly fruit preferred by bats, the bats
too will suffer shortages, and as Bonaccorso (1979) claimed, it
will be a factor limiting population size.
Summary
Seasonality of the food supply controls the reproductive
cycle of A. jamaicensis, with birth peaks timed to take
advantage of succeeding fruiting peaks. Previous studies
observed that larger species of bats took larger fruits and
smaller species took smaller fruits, suggesting food-limited
populations of canopy frugivores. Competition theory also
suggests that coexistence is possible if food particle size differs
by the ratio of 1.4: 1 estimated by earlier work. However,
small- and large-fruited species of figs are not uniformly
distributed in time or space, and the bats are adaptable enough
to take what is available.
Although fig trees bear fruit asynchronously, there is a peak
early in the dry season, a lower peak at the beginning of the
rainy season, and a low late in the rainy season. A 25 ha plot of
forest on BCI contained 49 F. insipida, which produced 34 full
crops per year during the study period, and 71 F. yoponensis,
which produced 64 full crops per year. If previous estimates of
40,000 fruits in an average full crop of either species are
correct, the 25 ha of Lutz Ravine could yield about 60,000 F.
insipida and about 100,000 F. yoponensis fruits per hectare per
year. This converts to about 170 kg dry mass of figs per hectare
per year for second-growth forest and averaged with the much
lower production in older forest, suggests an islandwide
production of roughly 100 kg dry mass of fruit per hectare per
year. Our calculations suggest that frugivorous bats consume
28 kg dry mass per hectare per year of this production.
Howler monkeys and kinkajous compete with bats for figs,
and guans, toucans, coatimundis, and other monkeys are
incidental competitors. Despite the good fit between numbers
of bats, consumption of figs, and supply of figs, the
reproductive cycle of A. jamaicensis seems not bound by the
cycle of fig production. Rather, reproduction seems geared to
take advantage of peaks of production of edible fruit in general,
and competition in times of short supply may be a factor
limiting size of populations of bats.

12. Appendix
Methods of Capturing and Marking Tropical Bats
The Bat Project on Barro Colorado Island (BCI) developed
an array of techniques and methods that facilitate and simplify
capturing and marking bats. This protocol evolved throughout
the first five years of field effort. To assist future projects
dealing with bats, we have outlined our methods in consider-
able detail. Additional useful tips on methodology relating to
many aspects of the study can be found in Kunz (1988).
Finding Bats
We quickly discovered that it was more productive to net for
Artibeus jamaicensis in the vicinity of trees bearing ripe fruit
than in sites selected at random. Fruiting trees often could be
located by the calls of noisy frugivores such as guans, parrots,
and monkeys by day and kinkajous by night. If the crop was
particularly large, the odor of fruit rotting on the ground often
carried on the breeze for some distance. We also searched for
the piles of pellets of pulp that stenodermatines spit out under
their feeding roosts after they have extracted the juices from the
fruit. Great numbers of pellets scattered over an extensive area
indicated a nearby fruit bearing tree used by large numbers of
bats.
Netting Stations
Our standard netting station consisted of ten mist nets, each
10 or 12 m long, strung between 3 m tubular aluminum poles.
Rarely, if space for nets was limited, we substituted one or
more 5 or 6 m nets. For transport we apportioned the 20 poles
into bundles tied securely at each end, and carried them over the
shoulder, resting between the horns of a pack frame. Two
persons could carry the poles and other paraphernalia required
for a capture station over a rough trail without undue stress, but
it was easier with three persons.
If possible, we placed the nets along a trail near a fruiting
tree, around the base of the tree, or on a ridge overlooking the
tree. As far as was possible, the nets were arranged in a zig-zag
pattern along trails with ends overlapping about 1 m, thereby
blocking as much of an underbrush-free area as possible.
We stretched the net shelf strings tight to minimize tangling
of large Artibeus, and high enough to keep heavy bats in the
lower shelf off the ground. These tactics facilitated the capture
of the larger bats, but somewhat diminished our chances of
catching smaller kinds.
Our marking station, always near the netting area, consisted
of a 3 x 4 m lightweight tarp stretched over a rope tied between
two trees to provide shelter; lightweight folding stools; and a
small plastic ground cloth for spare batteries, canteens, packs,
and other equipmenL All marking stations were temporary and
could be set up or taken down in a matter of minutes.
Catching Bats
We usually set nets five nights each week following a
schedule of two nights on, one off, three on, one off, but we
modified this schedule if circumstances dictated. Normally the
netting sessions began at dusk and ended when the bats quit
flying, regardless of light conditions. Sometimes we closed the
nets after an hour or two if netting was slow, but occasionally
we netted until dawn. When possible, we furled the nets during
showers.
We kept the bats in 20 x 30 cm bags made of Monk's Cloth,
a soft but strong open-weave fabric that would not chafe the
elbows, wrists, and knees of the bats and minimized overheat-
ing and suffocation. We kept empty bags handy on rope belts
and as we collected bats from the nets and bagged them, they
hung from the same belts. We never mixed species in a bag and
usually used a separate bag for each individual, although on
exceptionally busy nights we put two or three bats in a bag. We
hung the bagged bats in the marking station in hourly lots on
poles or lines strung close to the processors. Poles laid over
pack frames stuck upside down into the ground about a meter
apart made handy bag racks.
Because they might not have eaten before we caught them
and, therefore, might easily become fatally stressed, we
processed bats of the first hour promptly. Small bats, regardless
of capture time, were segregated and processed quickly. The
energy budget of small stenodermatines is so constrained that
they can deplete energy reserves to lethal levels in minutes.
We patrolled the nets constantly and removed tangled bats as
soon as possible. If the bats began to come in faster than we
could remove them, we closed nets as each was cleared until we
151
152 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
- 10
- 20-
dB - 3 0 -
8 16 24 32 40 48 56 64 72 80
FIGURE 12-1.?Sound spectrum of Audubon Bird Call, used to attract bats. From recording by James Fullard and
Jackie Belwood.
had only as many nets open as could be kept cleared. When the
catch slowed we reopened nets.
The distress calls of particularly vocal bats were useful for
attracting other bats into the nets. In the absence of such bats,
the squeaks of an Audubon Bird Call often were effective in
attracting bats. James Fullard and Jackie Belwood tested these
mechanical squeakers and found all the squeaks were in the
audible range, with no ultrasonic components (Figure 12-1).
The bird calls put out most of their energy at values between 8
and 16.8 kiloHertz (kHz) with a peak mean of 14.85 kHz.
Maximum frequencies ranged between 50 and 52 kHz. The
effectiveness of the bird call for bats may be limited by its
absolute intensity rather than its frequency output (bats squeak
louder).
Using folded capture bags as baffles that the bats might bite,
we seldom were bitten ourselves. Everyone handling bats was
protected with rabies vaccine.
Necklacing
Bats have proven difficult to mark without suffering serious
injury. Wing and interfemoral membranes are sensitive and
easily irritated. Toes are few and clipping them may interfere
with the bat's ability to roost. Ear tags tear out and may limit
maneuverability of the ear or obstruct reception of sonar
signals. Body size is too small for effective use of heat or freeze
brands. We needed a marking system that (1) would not
interfere with normal behavior; (2) could be easily and quickly
applied in the field; (3) could be easily and accurately
interpreted upon recapture; and (4) was durable enough to
supply the desired information about the bat throughout its
lifetime.
Previously, forearm banding was the method of choice for
marking bats. Partly because the side effects of forearm
banding proved even more disastrous to bats in the tropics than
in temperate zones, few long-term studies based on marking
tropical bats have been successful. Consequently, compara-
tively little is known about populations, longevity, movements,
seasonal and annual variations, and other aspects of demogra-
phy in tropical bats. This is a serious problem for biologists
studying bats because the majority of the species of bats are
exclusively tropical.
We tried and rejected a number of techniques for marking.
Eventually we settled on stainless steel ball-chain necklaces
carrying numbered aluminum bands as a safe and effective
device for marking tropical bats. We rarely found signs of
serious irritation from the necklace, and the loss rate of
necklaces is so low (6.6%) that we didn't consider it a problem.
The chain consists of smooth hollow balls closely linked by
dumbbell-shaped rods. An easily attached connector joins the
ends of a length of chain into a necklace. Ball chain is strong,
lightweight, and because it is flexible and swivels, it can not
kink. Chain is available in continuous lengths up to thousands
of feet. Although we used smooth, stainless steel ball chain, it
is also manufactured from brass, monel, copper, aluminum,
gilding metal, nickel-silver, and high carbon steel, all of which
come in a variety of finishes. The smallest size available is no.
00 with balls measuring 1.575 mm in diameter and a tensile
strength of 4.54 kg; the largest is no. 20, which has balls 9.525
mm in diameter and a tensile strength of 84 kg. We obtained
NUMBER 511 153
our chain from Ball Chain Manufacturing Company, Inc., 741
South Fulton Ave., Mount Vernon, NY 10550; telephone (914)
664-7500.
Mainly we used no. 3 (2.388 mm, 9.08 kg) stainless steel,
standard ball chain and no. 3 stainless steel connectors. No. 3
chain has 100 beads per foot. Five bats the size of A.
jamaicensis (which take a 20-bead necklace) can be marked
with one foot of chain. Five hundred feet of no. 3 chain will
mark about 2,500 bats. For the smallest bats, whose necklaces
would have less than 15 balls in no. 3 chain, we preferred no. 2
chain (2.083 mm, 7.264 kg).
Necklace lengths we used for each species are tabulated in
Table 12-1. Geographic variation and sexual dimorphism in
populations elsewhere may require adjustments in necklace
lengths for these and other species. The advantage of
necklacing is that it is harmless to bats. It should be emphasized
that this advantage is lost if the necklace is improperly fitted.
The necklace must not fit too snugly around a bat's neck. It
should be possible to slip the points of a pair of hemostats (used
to attach the necklace around the neck) under the closed
necklace. On most bats, the necklace should be loose enough so
that it can be slipped off over the bat's head with little
difficulty. The bat itself, however, usually will not be able to
remove the necklace because it will use only one foot or one
thumb at a time, thus causing the necklace to bind diagonally.
We have found that a bat will ignore the necklace within a few
minutes after it is in place.
For obvious reasons we did not mark juvenile bats with
necklaces smaller than those required for adults. Suckling
young and even some volant young, because of their small size,
cannot be necklaced. We also did not mark bats such as
Molossus and Centurio, which have skin pads or gular glands
on the throat. Chest glands are low enough on the torso not to
interfere with necklacing in Trachops, Tonatia, and Phyllod-
erma.
Anticipated numbers of necklaces of the lengths needed were
cut with small sidecutter pliers and a connector was attached to
one end of each before the capture operation. We found that
slightly opening the unattached end of the connector with
needle-nose pliers or hemostats made closure of the necklace
when wrapped around a bat's neck much easier. We had two
ways of storing necklaces. Our first method was to close
(fasten) each necklace and string those of the same size on a
large safety pin such as a diaper pin; each necklace has to be
opened before use. Our preferred method was to store the
unconnected necklaces by size in a flat, compartmentalized
plastic box such as those designed to store buttons, fishing
lures, or other small items.
At the time of marking, a numbered aluminum band was
slipped onto each necklace so that individual bats could be
recognized at recapture. The band should fit snugly on the
necklace, e.g., a no. IB band (inside diameter 2.769 mm) on a
no. 3 necklace (outside diameter 2.388 mm), so as to cause a
minimum of disturbance to the wearer. A large, loose-fitting
TABLE 12-1.?Necklace sizes for bats of Barro Colorado Island, Panama.
Numbers refer to the number of balls in length of chain. (* = a species that
cannot be necklaced.)
Species
Size
#2 Chain #3 Chain
Artibeus jamaicensis
Artibeus litwatus
Artibeus phaeotis
Artibeus watsoni
Carollia brevicauda
Carollia caslanea
Carollia perspicillata
*Centurio senex
Chiroderma villosum
Chrotopterus auritus
Cormura brevirostris
Desmodus rotundas
Glossophaga commissarisi
Glossophaga soricina
Lonchophylla robusla
Macrophyllum macrophyllum
Mesophylla macconnelli
Micronycteris brachyotis
Micronycteris hirsuta
Micronycteris megalotis
Micronycteris nicefori
Micronycteris schmidtorum
Mimon crenulatum
*Molossus coibensis
*Molossus molossus
Myotis albescens
Myotis nigricans
Noctilio albiventris
female
male
Noctilio leporinus
female
male
Phylloderma stenops
Phyllostomus discolor
Phyllostomus hastatus
Platyrrhinus helleri
Pteronotus gymnonotus
Pteronotus parnellii
Rhogeessa tumida
Rhynchonycteris naso
Saccopteryx bilineata
Saccopteryx Upturn
Tonatia bidens
Tonatia silvicola
Trachops cirrhosus
Uroderma bilobatum
Uroderma magnirostrum
Vampyressa nymphaea
Vampyressa pusilla
Vampyrodes caraccioli
Vampyrum spectrum
15
15
15
14-15
15
15
15
14
15
13
15
13
15
13
13
15
14
15
13-14
20-21
23
15
15-16
16-17
23-24
17
15
15
15-16
15
17
18
20
18
18
23-25
15
15-16
18
18
16
15
15
17-18
25
band may move about on the necklace, pinching hair and
otherwise irritating the bat's neck. Colored plastic bands may
be useful for distant recognition of individual bats, but because
154 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
bands soon work around to a stable position under the bat's
chin, they might not be readily visible. Some plastic bands
become brittle and break in as few as three or four years, so they
may not be as effective as the more durable aluminum bands for
longer-term studies of populations. Custom-made aluminum
bands can be obtained from Gey Band and Tag Co., Inc., Box
363, Norristown, PA 19404; telephone (215) 277-3280. Plastic
bands suitable for necklacing are available from Messrs. I.
Dennison and J. Warner, 116 Moor Crescent, High Grange
Estate, Belmont, County Durham, DH1 1DL, England.
Bats were most easily necklaced by two persons working as
a team. The processor removed the bat from the capture bag and
called out its identification, age, sex, and reproductive
condition. Usually grasped by its elbows between the fingers of
one hand, the bat was then held out toward the necklacer. The
person doing the necklacing recorded the data on a field form
and then selected a chain of appropriate length, slipped it
through a band, grasped the free end of the necklace between
the second and third bead with the tips of a pair of small
hemostats held in one hand, grasped the connector end of the
necklace with the other hand and, placing the connector behind
the bat's head, quickly passed the hemostats under the bat's
chin, slipped the free bead into the connector, and snapped it
shut. The processor then weighed the bat, released it, and
checked its capture bag for feces. With a little experience,
necklacing proceeded smoothly and quickly. When a third
person was available to record data, the operation was even
faster.
It is possible for one person to do the necklacing alone. The
necklacer holds the bat on his knee with one hand while
grasping the connector end of the necklace with fingers of that
same hand, the free end of the necklace can be brought around
the neck and fastened using hemostats held in the other hand.
We also have used a bat restrainer "bat package" made by
sewing 150 mm-long by 25 mm-wide, "hook" and "eye" strips
of Velcro back to back to facilitate solo marking. When the
Velcro is wrapped around a bat to bind its wings firmly to its
sides, the animal usually ceases struggling and the necklacer
can then fasten the necklace around the bat's neck.
When we recaptured a bat, we moved the band to the back of
the neck to facilitate reading, and then rotated the band with
fingers or hemostats to expose all of the numbers. To ensure
accuracy, we always read the number at least twice, by different
persons if possible, and the recorder called it back. Interpreta-
tion and recording of a band number can be the weakest link in
the mark-recapture process. A misread number is a wasted
capture.
Recording Data
Our recording system was designed for computer storage of
the data. Through a process of trial and error, we developed
data sheets that ensured standardized data, largely prevented
accidental omissions, and eliminated transcription except at the
computer terminal. All entries were made in waterproof black
ink with a Rapidograph or equivalent pen. Field forms were on
216 x 280 mm (8V2 x 11 inch) sheets held together on a
clipboard, which we carried between the netting station and our
home base in a zippered waterproof plastic pouch. We used
three forms: (1) a nightly cover sheet for general information
about the netting episode; (2) a field data sheet for individual
band entries; and (3) a nightly summary sheet for marks and
recaptures.
COVER SHEET.?We recorded general information about
each netting episode on the Field Data Cover Sheet (Figures
12-2 and 12-3). This included date, location, release site
(ordinarily the netting station), numbers and kinds of nets,
opening and closing times of nets, net hours, light conditions,
rain, fruit presence and evidence, presence of potential
predators of bats, and remarks about peculiarities of the
evening. This information was entered on the sheet whenever
appropriate during a netting episode. Our standards for this
form were as follows.
1. Locality: We identified capture localities to the nearest
0.1 km by their X and Y coordinates on a grid 100 km2, with
BCI at the center (Figure 12-4). This system allowed us to use
the coordinates of the locality as the site's code name for record
keeping. This system also made it easier to program for
computer plotting and for calculation of areas and distances. By
having BCI at the center of the grid (identified as point 50.0 x
50.0) we never had to deal with negative numbers. For
example, the Laboratory Clearing is "50.7 x 50.9," Armour
End on the opposite side of the island is "48.3 x 48.4," and
Bohio Ridge on the mainland is "48.9 x 54.3." To simplify and
speed the process we dropped the decimals from the six-digit
code when we recorded the data, but we restored them when we
entered the information in the computer. A constantly updated
gazetteer (Table 12-2) provided the locality code for each site.
We caught bats at 106 localities on BCI (plus 15 others on
the mainland and other islands)?far too many sites for
convenient analysis. Consequently, we segregated the 106
localities on BCI into 20 regional groups (Figure 12-5).
2. Time: We recorded time of capture in 1-hour incre-
ments on a 24-hour clock. We defined an hour as from 30
minutes before zero to 30 minutes after (e.g., 2000 h = 1930 to
2030). Although we removed bats from nets as they were
caught and tried to check all nets at the end of each hour, some
errors undoubtedly occurred when we were catching many bats.
At the marking station the bats from each hour were kept in
separate lots.
Times of opening and closing the nets were recorded to the
nearest quarter hour. If we required more than a quarter hour to
open or close nets, we recorded the times in quarter-hour lots or
recorded a median quarter-hour time.
For record keeping, the day began at daybreak and continued
through the succeeding night. Thus, the date did not change
(advance) at midnight.
3. Net Hours: Lapsed hours, minus rain time, equals catch
time, and multiplied by the number of nets equals the number
NUMBER 511 155
TABLE 12-2.?BCI Bat Project gazetteer.
Locality
Allee Creek
AMNH 1-2
AMNH3-4
Armour O(AVAO)
Armour-Zetek Junction (AVA 2.5)
Armour 6
Armour 9-11
Armour 14
Armour-Conrad Junction
Armour 20
Armour end
Balboa 2-3 (Balboa 1-4)
Balboa 6 Creek (Balboa 4-6)
Balboa 7 Ridge (Balboa 7-8)
Balboa 12 Creek
Barbour-Lathrop-Miller Shortcut
Barbour-Lathrop 16
Barbour Stream Station A (B-L 3.5)
Barbour Stream Station B
Barbour Stream Station C
Barro Colorado Island
Bohio Trail
Bohio Ridge (saddle)
Buena Vista (No. 9 front marker)
Cacao Cove
Cat Creek Cove
Chapman 6-9
Chapman 8-9 (FMC 8-10)
Chapman End (FMC 9-11)
Chilibrillo Caves
Conrad 1-2
Conrad 4
Conrad Creek
Donato 1-3
Donato 3-4 (Lutz Loop)
Drayton 2-3
Drayton 16
Drayton 18.5
Drayton Estero
Dump Cove
Fairchild-Wheeler Junction
Fairchild 5-7
Frijoles (Kidd's Place)
Frijoles Road
Fuertes Cove
Fuertes House (Nemesia Creek)
Fuertes Ridge
Gigante
Gigante Rancho
Giral Caves
Gross 9-10
Gross Point
Harvard 10 (Harvard Cove)
Lab Clearing (Snyder-Molino 0)
Lake 4-6
Lutz Creek (Lutz Creek-Lutz 3)
Lutz Creek mouth
Miller Creek mouth
Miller 1-2
Miller 4-5
Miller 7-8
Code
506x510
503 x 493
504 x 494
495 x 501
495 x 500
493 x 498
490 x 497
487 x 494
486 x 494
484x490
483 x 484
497x502
500x501
501x 500
504 x 497
499x510
500x517
503x510
502x514
503x515
000x000
488 x 543
489 x 543
501x 535
486x515
489x515
518x498
520 x 498
522 x 498
748 x 517
486 x 495
484 x 496
489 x 498
508 x 508
508x507
495 x 499
498 x 488
500x486
500x482
509x509
504x510
505 x 514
552 x 522
543 x 538
489 x 513
489 x 512
490 x 514
514 x 463
478 x 452
667x603
500 x 526
499 x 527
517 x 492
507x509
497x507
507 x 508
508 x 510
495 x 516
501x 507
499x508
495x511
Locality
Miller 8-10 and Nemesia 1
Miller 11-13
Miller 13-14
Miller 15-18
Miller Cove (outer)
Mona Grita Point
Navigational Aid No. 5
Navigational Aid No. 7 (Darien Island)
Nemesia B (Upper Nemesia Creek)
Nemesia 2
Nemesia 4
Orchid Island
Orchid Island No. 2
Pearson 0.5-3.5
Pearson Creek
Pena Blanca (No. 11 front marker)
Power Line Hill
Punta Carlo Quebrado
Schneirla 1-2 (New Wheeler 9)
Shannon 1 -2 (creek)
Shannon 6
Shannon 10
Shannon 13.5
Shannon 17
Snyder-Molino 0-2
Snyder-Molino-Lutz
Snyder-Molino 4
Snyder-Molino-Wheeler Junction
Standley 5
Standley 13 estero
Standley 13 ridge (PCS 12.5-14)
Standley 16 (PCS 15-16)
Standley 17 estero
Standley 19 estero
Standley 21 (Standley end)
Barbour-Shannon cutoff
Barbour 3 (TB 2-4)
Barbour 5 (TB 4-6)
Barbour 7
Barbour 9
Barbour 11 (TB 10-12)
Barbour 14-16 (TB-Hood Junction)
Barbour 20-21
Barbour end
VanTyne 0-1 - Barbour 10
VanTyne 2 - Big Tree
VanTyne-Hood-Chapman Junction
VanTyne-Shannon end
Wheeler 2-3
Wheeler 4
Wheeler-Miller Junction
Wheeler 12-14
Wheeler 15 (WMW-FD Junction)
Wheeler 20
Zetek 1-3
Zetek 3 (Zetek 2-4)
Zetek-Armour shortcut
Zetek 7
Zetek 13
Zetek 21 (JZ 20-22)
Code
494x512
493 x 513
493 x 515
493 x 516
493 x 520
512 x 474
599x465
575 x 445
490 x 511
492 x 512
491x512
497 x 528
496 x 527
494 x 503
489x511
461 x 522
507x511
534x464
500x506
503x506
503x501
503x499
507 x 497
507 x 494
506x508
505x507
504x507
503 x 507
483 x 500
479x511
479X510
478 x 512
479 x 513
479 x 516
476 x 516
504x506
505 x 505
507x504
508x504
510x504
512x504
515 x 505
520x505
526x506
511x504
511x502
514x497
508 x 493
504x509
503 x 508
502 x 507
496 x 502
496x499
497 x 498
493 x 500
490 x 499
491x 498
487 x 499
484 x 497
477 x 501
156 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
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158 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
4 7
4 6
4 5
4 5 4 6 4 7 48 49
2 3
kilometers
FIGURE 12-4.?Grid system of one kilometer squares used to identify localities on Barro Colorado Island and
surrounding mainland. Stars indicate canal range light towers. Those mentioned in the text are Pefia Blanca (near
46 x 52) and Buena Vista (50 x 53). Dashed lines on BCI trace approximate alignment of trails.
NUMBER 511
5 5
5 4
5 3
5 2
5 1
5 0
4 9
4 8
4 7
4 6
159
4 5
4 5 4 6 4 7 4 8 4 9 5 0 5 1 5 2 5 3 5 4 5 5
2 3 4
kilometers
FIGURE 12-5.?Capture localities (black dots) and locality groups (large circles) on BCI and surrounding
mainland used by the Bat Project, 1976-1980. Dashed lines show extent of locality groups.
160 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
of net hours. We treated a 5 or 6 m net as one half of a 10 or 12
m net.
4. Moon Phase: We recorded moon phase from the
calendar, adding the number of nights since the beginning of
the current phase.
5. Cloud Cover: CLEAR = sky cloudless; FEW CLOUDS
= sky 74 cloud covered; PARTLY CLOUDY = sky xh covered;
MOSTLY CLOUDY = sky 3A covered; CLOUDY = sky
completely overcast.
6. Light Conditions: VERY DARK = too dark to see
hands; MODERATELY DARK = light enough to distinguish
objects; MODERATELY LIGHT = light enough to see a
considerable distance; VERY LIGHT = light enough to read.
We estimated light conditions at the net station. Sometimes
we recorded combinations such as "VERY DARK until
moonrise, 2100, then VERY LIGHT;" or "MODERATELY
DARK during rain, otherwise MODERATELY LIGHT."
7. Rain: We defined rain as throughfall heavy enough to
wet the ground. We did not consider a fine mist, which
contributes only leaf drip, as rain. The rain categories we used
were: HEAVY = torrential, ground is covered with water, noise
of the rain drowns out all other sounds; MODERATE = rain of
average intensity, noisy, but not masking all other sounds;
LIGHT = drizzle, quiet, individual leaf drips can be distin-
guished; DRIP = leaf drip during mist or after a rain (noted in
our records but not qualifying as rain).
FIELD DATA SHEETS.?Data for individual band numbers
were entered on Field Data Sheets (Figures 12-6 and
12-7)?new marks on one set of sheets; recaptures on another.
Our form has 15 double-line spaces and we used each couplet
of lines for the record of one bat; the upper line for field data
and the lower line for a computer code. Data that allowed
mnemonic codes (e.g., age, sex, date, hour, and band number)
were entered as they were noted directly on the code line. The
remaining data (such as locality, species identification, and
female reproductive stage) were coded upon return to our
operations base, preferably during the same evening.
The columns on this form are organized into 17 data fields
separated by spaces rather than zeros. Computer entry for this
form was programmed to accept blanks in nonapplicable spaces
such as in items that applied only to one sex or the other.
Information standards for this form are as follows.
1. Identification of Species: From the outset we required
that inexperienced field personnel spend a day in the museum
reviewing a synoptic set of bats before going to Panama. The
banding kit carried each night included a key to the bats of the
lowlands of Panamd and a synopsis of the species known to
occur on BCI, with detailed descriptions and key characters of
each.
Personnel were instructed to save the first of any species not
known to occur on BCI as a voucher specimen to substantiate
its occurrence. With the exception of constant (but understand-
able) confusion of A. phaeotis and A. watsoni, data from
recaptures revealed surprisingly few inconsistencies, which
strengthens our confidence in the identifications.
For coding purposes, we alphabetized the list of species
known to occur on BCI and applied a simple numeric code, 1
to 56 to each kind. Fortuitously, A. jamaicensis was number 1
and several of the most common species had easily recallable
single digit numbers. Hindsight shows, however, that we
should have used more easily remembered alpha codes, which
quickly evolved in field parlance, such as AJ (= A. jamaicen-
sis), CC (= Carollia castanea), CP (= C. perspicillata), CV (=
Chiroderma villosum), UB (= Uroderma bilobatum), VC (=
Vampyrodes caraccioli), etc.
2. Sex: Sex was coded F for female and M for male.
3. Age: We based age standards on observation of
maturation in several generations of A. jamaicensis in our NZP
colony. These proved applicable to other species as well.
Although we looked at a number of characters, the most
important were ossification of the digital cpiphyses to
distinguish subadults from juveniles; evidence of reproduction
to distinguish adult females from subadults; and enlarged testes
to set apart adult males. Our full protocol for determining age
in A. jamaicensis was as follows.
Juvenile: Individuals that are 1 to 3 months of age arc
considered juveniles. The prime factor that distinguishes
juveniles from the other age groups is the epiphyses of the
fingers are open (unossified), with the joints swollen and
tapering. Epiphyses appear translucent when viewed before a
light. When the epiphyses of the last joint (usually on finger V)
ossify, the bat is classed as a subadult. Other important
characteristics of juveniles include a body size that is small at
first but then large; a gray pelage that is downy initially but
becomes smooth; tiny ( 5 x 3 mm or less), pale testes, with the
skin of the testicular region hairy (males); and tiny, pale nipples
that are hidden in hair (females).
Subadult: Individuals that are 3 to 12 months of age are
termed subadults. In subadults the epiphyses of the fingers are
closed (ossified) and knobby. In males, the testes are small (3
x 2 mm to 7 x 5 mm) and pale, with the testicular region hairy.
The nipples of females are tiny, pale, and hidden in hair.
Females are nulliparous. Other distinguishing characteristics
include a large body size and a smooth, usually gray pelage.
Adult: Individuals are considered to be adults when they
are 8 to 12 months of age or older. The epiphyses of the fingers
are closed and the joints knobby. In males, the testes are
medium-size to large ( 7 x 4 mm or more) with the overlying
skin sometimes pigmented and naked. In females, the nipples
are small (never tiny), medium-size, or large and may be dark
and naked. Females are parous. By these criteria the infrequent
nulliparous female beyond a year in age would be recorded as
a subadulL Other important characteristics include large body
size, dark gray or brownish pelage, and tooth wear may be
obvious.
NUMBER 511 161
3
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162 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
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NUMBER 511 163
4. Reproductive Categories: Females: We used these
reproductive categories for females: no reproduction, pregnant,
lactating, postlactating, pregnant and lactating, and young on
nipple.
Pregnancy: The abdomen of every female, regardless of
age and reproductive condition, was palpated to detect
pregnancy in the following manner. The bat was grasped by its
elbows with the right hand, with its abdomen facing left. The
left thumb and index finger were used to gently palpate the
abdomen. A fetus could be felt by gentle pressure (down, back,
and inward) on the abdomen, just posterior to the ribs. If the
head of a fetus (a hard lump) could be felt, the bat was palpably
pregnant. Abdominal distention also may be caused by food or
gas, so it was necessary to feel the fetal skull to be sure of a
pregnancy.
In A. jamaicensis, a fetus with a crown-rump (CR) length of
30 to 35 mm or more will distend the abdomen, and the CR
length can be measured with surprising accuracy (tested by
later dissection and direct measurement of the fetus in bats that
died in handling) with a millimeter rule. When a fetus is too
small to distend the abdomen its CR length can be estimated. It
is possible to be misled by the left kidney, which can be felt
easily and mistaken for a small fetus. The left kidney is about
10 x 5 mm in its greater dimensions and can be felt and moved
by gentle pressure on the abdomen close to the backbone.
Familiarity with the position and shape of the kidney can be
gained by palpating male bats. A bat was not recorded as
pregnant unless both kidney and fetus could be felt.
Lactation: Lactation was determined by expression of milk
from a nipple. A bat was presumed to be postlactating if nipples
would not express milk, but were large, flabby, and surrounded
by naked skin. This was the only criterion used early in the
project. Later on, we made a more accurate determination.
Postlactation was recorded if no milk was present, areolas were
naked or new hair was growing in, and nipples were any size.
Nipple Condition: The parameters of nipple condition we
recorded were size, color, and presence of areolar hair. Because
these vary with age and season, as we learned from our NZP
bats, they provide accurate clues to the reproductive state. For
example, TINY-LIGHT-HAIRY can only be a nulliparous bat;
MEDIUM-LIGHT-HAIRY is a preparous adult bat; LARGE-
DARK-NAKED goes with lactation; MEDIUM-DARK-NEW
HAIR is postlactating.
Nipple size was measured with a template (Figure 12-8)
based on measurements taken on the A. jamaicensis in the NZP
colony. TINY nipples are immeasurable, and they cannot be
pinched. They are characteristic of juvenile and subadult
(nulliparous) bats. SMALL nipples vary from 0.5 to 3 mm in
length and from 1 to 6 mm in diameter at the base. MEDIUM
nipples vary from 4 to 6 mm in length and from 5 to 7 mm in
diameter. LARGE nipples vary from 7 to 10 mm in length and
from 5 to 10 mm in diameter.
Nipple color was recorded as LIGHT or DARK. All
s
1/2 X
T l
MA
1
A J
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LL
3 X 6
/ \
NIPPLE GAUGE
UNMEASUR
M E D I U M
6 X 7
4 X 5
L
7 X
J
A
A
5
V
BLE
RGE
10 X 10
FIGURE 12-8.?Gauge used to determine size of nipples of Artibeus
jamaicensis on BCI.
nulliparous and some adult A. jamaicensis have pale, unpig-
mented, i.e., LIGHT, nipples. Some parous individuals have
nipples colored with tan to fuscous pigmentation, which may
vary from a few flecks of color to the entire nipple. Any
pigmentation, regardless of amount, was recorded as DARK.
Although the distribution and intensity of pigment might vary
seasonally, any bat with pigmented nipples was assumed to be
adult.
Nipple hair refers to the areolar region, which we described
as HAIRY, NAKED, or having NEW HAIR. The areola is
HAIRY in all nulliparous bats, and NAKED just before, during,
and following lactation. NEW HAIR, usually conspicuous
because its gray color contrasts with the drab brown older hair
of the chest, grows in as the nipples recede in size following
lactation.
Vulvar Coloration: We recorded the color of the vulva as
LIGHT, DARK, or BLACK. Nulliparous bats usually have a
pale (LIGHT) vulva. At parturition and during estrus the vulva
sometimes becomes heavily pigmented and BLACK. Follow-
ing estrus the coloration fades to fuscous (DARK) and
eventually only the vulval margin is pigmented (LIGHT).
5. Reproductive Categories: Males: Size and appearance
of the testes are clues to age and reproductive condition (Figure
12-9). We measured the approximate length and width of testes
with a millimeter ruler. Size of testes in A. jamaicensis varies in
juveniles from too small to locate, up to about 5 x 3 mm. Our
most frequently recorded dimensions on juveniles were 3 x 2
and 4 x 2 mm. Size of testes in subadults varies from 3 x 2 mm
to 7 x 5 mm (most frequently noted measurements are 5 x 3
mm and 6 x 3 mm), overlapping juvenile size at one extreme
and adult size at the other. Size of testes in adults varies from 7
x 4 mm to 13 x 7 mm and occasionally larger. In adults, size
varies seasonally, being largest when females are in estrus.
164 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
13
12
11
E 10-
1 9
O 7
z
LU 6
5
4
3
n m m
D n ?
? n
2 3 4 5 6 7
WIDTH (mm)
Testes in the shrinking (regressed) stage sometimes resemble a
deflated football. Loss of hair on the skin overlying the testes
(not a true scrotum) and increased pigmentation of the
testicular skin might reflect sexual activity. We recorded the
skin color as LIGHT, DARK, or BLACK.
6. Mass: We weighed bats with a Pesola spring balance
having a 300 g capacity. The bats were restrained in a clean
bag, which we weighed empty several times during the evening
to make certain the mass had not changed. We recorded all
masses only to the nearest gram, assuming that greater accuracy
was unrealistic.
7. Necklace Band Damage: Because a bat can reach its
own necklace only with its feet and thumbs, we have attributed
damage to necklace bands to be the result of grooming by a
roost partner. Because grooming behavior varies from species
to species, it is worthwhile to record the extent of damage to
bands. Damage was described as NONE, LITTLE (few
scratches), MODERATE (definitely chewed), EXTENSIVE
(almost illegible), or ILLEGIBLE.
8. Other Data: We recorded notes on wounds, hair loss,
feces contents, apparent stress, and other information on an
individual in column 42 (other data).
NIGHTLY SUMMARY SHEET.?This summary sheet (Figures
12-10 and 12-11) lists the nightly catch by new marks and
recaptures by hour and species. New marks were recorded in
the upper triangle of a pair and recaptures in the lower triangle.
Recaptures were always circled to emphasize and highlight
them. Totals were computed by species and by hour, and bats
per net hour was calculated by dividing total number of bats
captured by total number of net hours. For A. jamaicensis, the
catch was further subdivided by age and sex, and adult
recapture rate was calculated by dividing the number of adults
recaptured by the total number of adults caught.
FIGURE 12-9.?Variation in testis size with age in a captive colony of
Panamanian Artibeus jamaicensis. Circles represent juveniles; squares,
subadults; and dots, adults.
NUMBER 511 165
NIGHTLY SIR-MARY OF BAT CATCH
)ATE: LOCATION: NETS SET:
Hoars begin on half hoar
Captare/Re japture isp0 JooO A/CO 2200 Z*0O 0/00 OidO O'/OO ObOO
ARTIBEUS JAHAICENSIS
ARTIBEUS LITURATUS
ARTIBEUS PHAEOTIS
ARTIBF'JS WATSONI
CARULLIA C A S T A N E A
CAROLLIA FERSPICILLATA
KECRONYCTERIS HERSUTA
PHYU.OCTOMUS DISCOLOR
PTERONOTUS PARIELLII
TONATIA BIDE!B
TONATIA SILVICOLA
URODERMA BIL03ATUH
VAI4PYRESSA NYI4PHAEA
V.4MPYR0DES CARACCIOLI
HQTRLY TOTAL
Catch suinmary, A. jamaicensis (Caature/itecapture)
FLT ALE
MALE
Mark /Rec
Total
t-pecies
Total
AD SAD JUV
hark/Kec
total
TOTiJ, BATS CAPTURED:
bnTS Pbli UET HOUR:
RECAPTURES:
REPEATS:
ADJI.T RECAPTURE RAW
FIGURE 12-10.?Nightly summary sheet for a netting episode.
166 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
NTP.HTT.Y SUMMARY OF BAT CATCH
jNETS SET;
 [ oLOCATION;
Hours begin on half hour
Capture/Recapture tc?o loo Jooo ttx> 2200 l0O V0OO/00 %CO >*!/
ARTIBEUS JAMAICEKSIS
ARTIDEUG LITUnATUS
ARTIBEUS PHAEOTIS
CARULLIA CASTANEA
CAROLLIA PERSPICILLATA r
MICROinrCTERIS ULB3WA
PHYLLOSTOMUS DISCOLOR
PTERONOTUS PARNELLII
TONATIA HIDENS
TONATIA SILVICOLA
DILODATUM
NYMPJIAEA
y
y
y
y
HQJRLY TOTAL
Catch suiomary, A. jamaicensis (Capture/Recapture)
FEU ALE
MALE
Mark/Rec
Total
bpecxes
Total lp_
AU SAD JUV
Hark/Rue
total
TOTAL BATS CAPTURED:
B H T S PER NET HOUR:
<fO RECAPTURES:
REPEATS:
AU'JI,T RECAPTURE RATE:
FIGURE 12-11.?Completed nightly summary sheet.
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