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Chiroptera Neotropical 15(1), July 2009
Maintenance of the haematophagous bat Desmodus rotundus in captivity
for experimental studies on rabies
Marilene F. de Almeida¹, Caroline C. Aires² Luzia F. A. Martorelli¹, Rodrigo F. de Barros¹ and Eduardo
Massad³
1. Zoonosis Control Center of São Paulo Municipality. Rua Santa Eulália, 86 – Santana - São Paulo,
Brasil – CEP 02031-020.
2. Zoology Museum of São Paulo University - CP 42694- CEP 04299-970.
3. School of Medicine. The University of São Paulo LIM 01 – HC/FMUSP, Av. Dr. Arnando, 455 –
Departamento de Informática Médica - São Paulo, Brasil - CEP 01246-903 and Department of Infectious
and Tropical Diseases (Hon. Prof.), London School of Hygiene & Tropical Medicine, London, UK.
* Corresponding author. Email: [email protected]
Abstract
Current knowledge concerning rabies transmission by the haematophagous bat Desmodus rotundus is
considerable. However, many aspects of the relationship between haematophagous bats and rabies still
remain uninvestigated or contradictory. In an attempt to investigate some of these aspects, our group
designed a cage system developed for the purpose of experimentally investigating rabies infections and
the oral rabies immunization of haematophagous bats. The cages are made of polycarbonate, a transparent
material that allows for total visualization of the bats for observation, photos and video monitoring and
resistant to effects to bats excreta. Nine cages with independent air supply and exhaust systems are
maintained on a stand. A prefilter unit using inner and outer HEPA filters guarantees air supply to bats
through the cage interior, and air exhaustion provides for safe conditions for researchers. Drinking bottles
are located externally. Adequate consumption of defibrinated blood, weight maintenance, low bat
mortality (16.4%) and longevity are demonstrated herein. The maintenance of bats in these cages
decreases the necessity of handling them and is consistent with the conclusion that the bats adapt well to
captivity in this type of cage.
Keywords: cage, captivity, Desmodus rotundus, rabies, vampire bats.
health and breeding conditions (Greenhall 1935;
Wimsatt and Guerrieri 1961; Wimsatt et al. 1973;
Barnard 1995). In previous studies, the purpose of
the cage was to facilitate studies investigating
reproduction, behaviour and bat biology, but the
design of such cages did not consider biosafety
issues. These issues are critical, especially for
such rabies studies as those attempting to
determine the dose of rabies virus lethal to this
species, the antibody response following
experimental rabies infection, routes for
immunization against rabies, and the possibility
of rabies virus aerosol formation (Constantine
1962; 1967).
The purpose of the present project was to
develop a cage system for bats that permits
experimental studies of rabies in captivity
(Almeida et al. 2005a, b, Almeida et al. 2008),
while equally considering the adaptation of the
bats to captivity, essential for obtaining reliable
results, and the biosafety precautions needed to
protect laboratory staff.
Introduction
Several studies of antigenic typing and
phylogenetic analysis of the rabies virus have
indicated that bats are one of the most important
vectors and/or reservoirs of rabies in the world
(Nadin Davis et al. 2001, Krebs et al. 2005,
Schaefer et al. 2005, Velasco-Villa et al. 2006,
Kobayashi et al. 2007). Whereas rabies viruses
associated with insectivorous bats were involved
in 32 out of 35 (91%) human rabies cases that
occurred in the United States from 1958 to 2000
(Messenger et al. 2002), the haematophagous bat
Desmodus rotundus was associated with 136 out
of 230 (59%) human rabies deaths reported in the
Latin America from 2004 to 2007 (PAHO 2008),
including outbreaks in northern Brazil that
totalled 64 deaths (da Rosa et al. 2006; Barbosa et
al. 2008). Additionally, as a rabies vector,
haematophagous bats may cause heavy economic
losses in the livestock industry in many Latin
American countries (Ito et al. 2001; Favoretto et
al. 2002).
In 1932, Clark and Dunn maintained D.
rotundus in captivity for the first time using
defibrinated blood. Many studies have shown that
these bats can be introduced successfully into the
laboratory and maintained in numerous types of
cages for prolonged periods in apparent good
Material and methods
The D. rotundus bats used in this study were
collected in caves and in abandoned buildings
from cities in the states of Minas Gerais and São
Paulo, southeastern Brazil, between July 2001
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Chiroptera Neotropical 15(1), July 2009
and February 2004. A total of 195 specimens (80
males and 115 females) were collected.
The bats were transported in individual cotton
bags measuring 25x30cm. They were weighed
using a dynamometer of one Newton.
All personnel who handled bats wore individual
protection equipment and had been immunized
against rabies; moreover, their titre of rabies
antibodies was monitored every six months, as
recommended in the São Paulo State technical
manual (2003). The ethics committee at São
Paulo University authorized all experimental
procedures and the capture and captivity of bats
was authorized by a Brazilian institution
responsible for wild animal care (Instituto
Brasileiro do Meio Ambiente, IBAMA).
Bats were divided by sex and capture location
into groups varying from 2 to 15 individuals. The
groups were maintained in captivity for a period
varying from four months up to one year. Once in
captivity, bats were identified using a nylon collar
and a designated letter (secur-a-tie®-08350 Avery
Dennison, USA) (Figure 1).
the upper screen permitted accommodation of the
bats in accordance with the behavior of the
species.
The cages were placed on a rack, which holds
nine cages, made of PVC and polypropylene
(Figure 2), with two independent air handling
systems: one for air supply and the other for air
exhaustion. The external air was sucked into an
axial motor and passed through a prefilter unit
(G3, retention of 97% of particles measuring 3 to
7μm to increase the life span of the main filter).
The cages were closed with aluminium lids - the
upper lid was doubled so that an air filter unit
(ALA 100) could be located between the upper
aluminium lids. Outgoing air passed through this
filter and was released to the outside. The air
turnover rate in the cage was 50 times per hour,
according to the manufacturer of the cages
(Alesco® São Paulo, Brazil) (Figure 3).
Figure 1: Collar and letters used on the bats for
identification.
The cages were maintained in an airconditioned room. Every day the minimum and
maximum temperature of the room were noted.
Light was turned on for two or three hours a day
whilst the room was cleaned, food was provided
and any technical procedures were performed.
Once a week the bats were weighed and
examined. During the day the room received
direct, low-intensity illumination through two
windows covered with a screen (mesh size 0.2
cm).
The cages were cylindrical (40cm in diameter
and 50cm in height) and made of polycarbonate,
with reinforcement added to the PVC area in
contact with faeces, urine and blood. The cages
were provided with aluminium-wire (mesh size of
0.5cm) screens. The lower screen permitted
separation of the bats from their excrements and
Figure 2: Cylindrical form cages for Desmodus
rotundus made of polycarbonate, with
aluminium-wire screens at their extremities. Air
435
Chiroptera Neotropical 15(1), July 2009
supply and exhaustion system integrated through
the interior of cages.
Figure 3: Details of the locations of the ventilation system and the attached feeding bottles.
Bats were fed with defibrinated swine blood.
The swine blood was obtained weekly from a
slaughterhouse, defibrinated and stored at 2-4°C.
Under these conditions, the blood remains usable
for a week; after this time, any remaining blood
was discarded. Frozen blood was also used
occasionally. Once a week, the bats were
provided defibrinated blood supplemented with
vitamins at a concentration of 1ml per litre of
blood (Clusivol® Wyeth-Whitehall Ltda.).
Once a day, 25 to 30 ml of blood per bat was
provided at 25-30°C in the late afternoon. The
bats were fed using external plastic bottles,
similar to the models used with other laboratory
animals (Beiramar, BBP250 São Paulo, Brazil),
which were removed during the day, immersed in
1% sodium hypochlorite and then washed in
running water.
The statistical test applied was the chi square
uncorrected test at the 95% confidence interval.
The test was run using the software EPI INFO 6.0
to compare the mortality between large groups
(more than 8 animals in a cage) and small groups
(less than 8 animals in one cage) and to compare
the weights of females and males.
significant difference occurred in mortality
between small and large groups (p=0.35; 95%
CI).
The average daily consumption of blood was
20.1ml, with a range of variation between 15.1ml
and 29.1ml. The average daily consumption
among groups of males was 20.3ml (+/- 2.0ml).
The average daily consumption among groups of
females was 20.0ml (+/- 2.1ml). The average
daily consumption was 20.1ml for large groups
and 25.3ml for small groups.
The average weight of adult males was 28.6 g;
with a range of variation between 25.4 and 32.5 g.
The average weight of nonpregnant adult females
was 33.4 g, with a range of variation between
30.6 and 38.7 g. The average weight of pregnant
females was 54 g, with a range of variation
between 48 and 60 g. The majority of
nonpregnant females (88.9%) had gained weight
by the end of the captivity period (an average of
1.93 g). In contrast, the majority of males (76.5%)
had lost weight (on average 2.42 g) by the end of
the captivity period. The difference between the
increase in weight of females and the decrease in
weight that occurred in males was significant (p=
52.14; 95% CI).
The nylon collar used for bat identification
caused local inflammation in 11% of the bats.
Throughout the experimental period, 33 bats
showed signs of being bitten by other bats (17%).
The regions of body most frequently affected
were the head (34%), the face (27%; eye, chin, lip
and nasal region), scapula (17%), ear (15%), the
thumb (5%) and the patagium (2%). The wounds
Results
Of the 195 total bats that had been captured
throughout the experimental period, 32 bats died:
the majority (23 bats, 72%) during the first 10
days of captivity; seven due to low weight during
the winter, and two after fighting with other bats.
Total mortality comprised 16.4% and occurred in
both large and small groups of animals. No
436
Chiroptera Neotropical 15(1), July 2009
received no medical treatment and healed in two
to three days.
The average minimum temperature in the room
was 20.7ºC and the average maximum
temperature in the room was 23.8ºC. The relative
humidity in the room ranged from 55% to 65%.
blood but did not relate this to the amount of
blood consumed; hence it became impossible to
compare blood consumption in our captivity
study with that of other studies.
When bats are maintained in small groups or in
isolation, the average daily consumption of blood
tends to be higher, as in this case, because there is
no competition for food. Under natural
conditions, feeding is an individual performance
and the competition for food is not a restrictive
factor; however, in captivity, the cages are
collective and the bats must share food. The
inevitable competition, in particular among males,
could reduce the average consumption of food per
bat. Also, fights among females did not occur
with the same frequency that they did among
males, and it was observed, on a few occasions,
that the females regurgitate blood for other
members of the group.
The average daily consumption of blood was
20.3ml for males and 20ml for nonpregnant
females, representing 71% and 60%, respectively,
of their total body weight, considering the
average weight of adult males and nonpregnant
females. Busch (1988) reported that vampire bats
in captivity consumed an average of 60% of their
body weight in blood over 30 minutes and
Wimsatt and Guerrieri (1962) demonstrated that
captive bats ingest large quantities of blood,
sometimes exceeding 50% of their body weight.
The temperature in the room was chosen based
on previous studies (Wimsatt and Guerrieri 1962)
using temperatures ranging from 21ºC to 25ºC. It
was also considered that the average ambient
temperatures of roosts are between 21ºC to 23ºC
(Flores-Crespo and Sota 1991). However, it is
possible that the room temperature influenced the
weight of the bats during the winter. A decrease
in weight, along with the death of individuals
with low weight was also observed, the majority
of cases occurring in males. The capacity for
thermoregulation in D. rotundus is marginal
(Wimsatt 1969). In the presence of lower
temperatures, bats must expend a higher amount
of energy than they can afford, simply for the
maintenance of normal body temperature;
particularly when bats are kept in small groups
(Delpietro and Russo 2002).
Water was provided for the first 21 days of
captivity. However, it was not consumed and was
thereafter removed. Results of investigations into
the vampires’ water requirements have been
variable. Altenbach (1981) reported that captive
specimens of the haematophagous bat Diphylla
ecaudata drank no water in captivity during 161
days of observation. Wimsatt and Guerrieri
(1961) observed captive D. rotundus to drink
little free water for a long as two years.
Accordingly, it is evident that defibrinated blood
provides the bats’ requirements for water;
Discussion
Air supply and exhaustion through the interior
of cages were implemented in consideration of
the possibility of aerosol formation by the rabies
virus (demonstrated by Constantine 1962; 1967),
and the high concentrations of rabies virus used in
experimental infection and vaccination studies
(Almeida et al. 2005a, b; Almeida et al. 2008). In
addition, the system diminishes the characteristic
smell of bat faeces and urine.
Initially, groups consisting of small numbers of
bats were maintained. These numbers were
progressively increased in number (2 to 15) to
establish the adequate number of bats per cage.
Eight to ten bats seemed to be the ideal number
per cage, so this range was adopted as the
standard. When 8 to 10 bats were housed in a
cage, two bottles of blood were sufficient to
ensure adequate feeding, but for higher densities
per cage, three or four bottles were required.
External feeding bottles were chosen so that it
was not necessary to open the cage to daily feed
the bats. Bottles are preferable to open dishes or
bowls used in other captivity projects (Wimsatt
and Guerrieri 1962) as they limit contamination
of the blood with the faeces and urine of the
animals.
In the captivity system described herein bats
fed rapidly, in agreement with previous reports
(Wimsatt 1969; Busch 1988). Within 10 to 30
minutes the bottles were emptied. In general, for
the first two days, the bats refused to accept food;
however, blood consumption increased rapidly,
stabilizing after one to two weeks of captivity.
Swine blood was chosen as the food source
because was most easily obtained in sufficient
quantity to keep the animals. Swine blood is
among the most preferable for this bat species
according Goodwin and Greenhall (1961), and it
was used successfully by Setien et al (2002). As
bats feed directly from mammals in nature, their
food is presumably nearly always at the standard
mammalian body temperature. Hence, all blood
was warmed to 25° - 30°C before being
presented.
According to Wimsatt and Guerrieri (1962) a
daily blood consumption average of 15 to 16ml is
sufficient to maintain vampire bats in captivity.
Greenhall (1935) reported that captive vampire
bats consume an average of 10 to 25ml of blood
each evening; however, they did not relate this
value to the volume that was offered. Setien et al
(2002) reported that bats received 15 to 20 ml of
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Chiroptera Neotropical 15(1), July 2009
1962; Barnard 1995; Delpietro and Russo 2002)
for defence and in social interactions. Levels of
dominance are determined by fights among males
for access to the preferred female roosting sites
(Wilkinson 1985; Lord 1992). The rates of
aggression can reflect this dominant behavior and
could explain why the same bats were bitten
many times, while others never showed any bites.
As expected, the region of the body most
frequently affected was the head and face.
Another explanation is that due to the cage size
restriction, mothers had great difficultly in
protecting their young, and babies were bitten by
adults, as previously observed by Winsatt and
Guerrieri (1961) and Greenhall (1935). Generally
the wounds completely healed within two or three
days; however, two bats died after fights as a
result of their wounds. Some groups showed one
dominant bat that refused to share the food with
the others in the group.
It was not possible to compare the mortality
rate obtained in this work with rates found for
other captivity studies of D. rotundus due to a
lack of previously published data. For Artibeus
lituratus and Sturnira lilium, the mortality rate in
captivity is 28% and 50%, respectively
(Rasweiler and Ishiyama 1973); for Glossophaga
soricina the mortality rate is 11% in captivity and
in Carolia perspicillata the mortality rate in
captivity is 7% (Rasweiler and Bonilla 1972). It is
not possible to compare the rates of mortality
among species of bats maintained under different
captivity conditions.
It was not the aim of this study to evaluate
reproduction in D. rotundus and the survival of
young bats in captivity; however, among the 115
females, 40 (34.8%) were pregnant, all of whom
conceived prior to capture. Of these, 6 females
died in the adaptation period, 16 pregnancies
ended in miscarriage, 6 premature young survived
less than 12 hours, 8 survived less than 30 days
and 4 lived to adulthood. Most of the miscarriages
(91.7%) occurred between one and two months
after the introduction of the females into
captivity, during the adaptation period. According
to Wilkinson (1985), the infant mortality of D.
rotundus in nature is 54% (Wilkinson 1985).
A major disadvantage of the air supply and
exhaustion system of the cages is the cost. The
Hepa filters cost approximately 150 dollars each,
which is moderately expensive, and have to be
changed every six months. However, these cages
are extremely suited to use by a group of
researchers in many studies; the great durability
of the cages, the quality of observation enabled by
photos and video monitoring, and the built-in
biosafety precautions compensate for this
expense.
The adequate consumption of defibrinated
blood, low bat mortality (16.4%), longevity,
however, according to Busch (1988), bats
consume 38% less blood when provided with free
access to water.
In the first week of captivity, the bats would
feed neither when the lights were on in the secure
environment nor in the presence of humans, but
after a few days they accepted food under these
conditions. Normally, the bats fed immediately
after being provided with blood. Only two groups
of seven and eight males never accepted food in
the presence of humans or in a lit environment,
even after five and six months of captivity,
respectively. When the blood was provided, these
groups of bats waited until the lights had been
turned off and the people had withdrawn from the
room. They then descended to feed, but they
always remained alert, and at the slightest sound,
they returned to the upper screen. The great
majority of bats, however, descended to the lower
screen and waited near the drinking place at
feeding time.
As stated in the literature, on average, mature,
nonpregnant females were heavier than adult
males. In our captivity their range of weight
variation was 30.6 to 38.7g, higher than that
observed (29 to 33g) by Wimsatt (1969). Among
males, the average body weight was 28.6 g, with
a range of variation between 25.4 and 32.5 g.
Although the majority of males (76.5%) had lost
weight (on average 2.42 g) by the end of the
captivity period, their average weight was similar
to that observed by Bush (1988) (30.1 g) and
Wimsatt (1969) (29.1 to 30.8 g).
Polycarbonate was chosen as the cage material
because it is transparent, allowing for full
visualization of the bats for observation, photos
and video monitoring. Also, this material was
resistant to the corrosive effects of bat excreta.
Faeces and urine from bats were copious. Urine
flow begins promptly after the onset of feeding.
Ammonia is corrosive to many types of material,
but the aluminium screens used in the cages were
resistant to the effects of the excreta. The
aluminium-wire was easily removable, facilitating
cage cleaning. When the lower aluminium screens
were immersed in 1% sodium hypochlorite for 20
to 30 minutes for disinfection, the excreta were
completely dissolved. The cages were washed
with water and washing powder.
It has been reported that bats are usually
heavily infested by ectoparasites of several
species (Wimsatt and Guerrieri 1961; Greenhall
1935). In our captivity study, only one species of
parasite was detected during a short period, albeit
in large numbers. We identified it as Necrobia
rufipes, a beetle (Coleoptera) of the Family
Cleridae. N. rufipes is a necrophagous insect that
is most likely attracted by the smell of blood.
Haematophagous bats present naturally
aggressive behaviour (Wimsatt and Guerrieri
438
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Acknowledgements
The authors are grateful to Carlos Campanerii
at the Zoology Museum of São Paulo University
and the Entomology Department at CCZ-SP for
identification of the Coleoptera. The following
people provided volunteer field assistance for bat
location and capture: Carlos Alberto Venésio
Gomes of the Vigilância Sanitária of
Paraisópolis-Minas Gerais; Alberto Dangeri of
the Prefeitura Municipal de Itatiba; and Luis
Carlos Ismerin and José Carlos Pinto of the
Escritório de Defesa Agropecuária of Sorocaba,
São Paulo. The authors are also grateful to Vilma
A Duarte Sanches, Valtair Santana and Ruberval
da Silva of the University of São Paulo School of
Medicine. The entire article was revised by a
native English-speaking scientific text editor.
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