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Geographic Translocation of Bats: Known and Potential Problems

posted Jan 4, 2017, 3:56 AM by Al Schema   [ updated Aug 30, 2017, 7:51 AM ]

Geographic Translocation of Bats:
Known and Potential Problems
Denny G. Constantine*

Natural, accidental, and intentional translocation of bats,
both intra- and intercontinentally, has been documented. Some
bats have been translocated while incubating infectious diseases,
including rabies or related lyssavirus infections; others
have escaped confinement en route to or at their destinations,
while others have been released deliberately. Known events
and potential consequences of bat translocation are reviewed,
including a proposed solution to the attendant problems.

Among the many potential consequences resulting from the
geographic translocation of life forms is the spread of
infectious disease organisms harbored by that life form. This
consequence was demonstrated long ago by the early devastation
of native American human populations caused by pathogens
inadvertently introduced by European explorers.
Similarly, wildlife rabies outbreaks occurred recently in the
United States after foxes, coyotes, and raccoons were translocated
to restock areas where these animals are hunted for
sport. Wild populations of introduced species can also become
common disease vectors where few or none existed before,
such as the current role of Indian mongooses (Herpestes javanicus)
in rabies transmission on Caribbean islands (1), or
they can become predators of native species, for example, the
wildlife destruction that occurred after ferrets and stoats were
introduced into New Zealand (2).
Bats have been translocated through natural, accidental,
and deliberate means. Pathogens associated with bats, such as
Rabies virus (RABV) and related lyssaviruses (3–6), can cause
disease after protracted incubation periods, ensuring the
extended survival of the host and parasite during periods of
translocation. Many bat species enter a hibernationlike state in
a cold environment, which further prolongs survival. In this
article, I describe some occurrences of bat translocation (published,
as well as previously unreported) and the potential consequences
of that translocation, as the basis for suggesting
preventive measures to alleviate the problems that accompany
the relocation of bats across the world.

Translocation of Bats
Natural Translocation
Some species of bats hibernate at the approach of cold
weather; other species migrate to warm areas instead. Bats that
migrate along coastlines take shortcuts over water and are
apparently blown far out to sea at times. Many North American
migrant bats have been found in Bermuda, 1,046 km east
of North Carolina, United States, during fall and spring migrations,
evidently having been blown there by wind along with
waves of migratory birds (7). These translocated bats include
Hoary Bats (Lasiurus cinereus), Red Bats (L. borealis), Seminole
Bats (L. seminolus), and Silver-haired Bats (Lasionycteris
noctivagans), all species from which RABV has been isolated
(8). Hoary Bats are also occasionally found in rabies-free Iceland,
also possibly blown there by the wind; one bat was captured
in the Orkney Islands, off rabies-free Scotland (9).
Similarly, Hoary Bats are sometimes found in the Galapagos
Islands, 966 km off the west coast of South America (10).

Translocation after Landing on Ships

Exhausted bats flying far at sea both individually and in
flocks have been reported to alight on ships and be transported
to unintended destinations. Most records are from the North
Atlantic Ocean and involve Red Bats and Silver-haired Bats
(11). A Southern Yellow Bat (Lasiurus ega) landed on a ship
over 322 km from the coast of Argentina (12). A “fruit-destroying
bat” was reported sleeping in the rigging of a ship upon
arrival in Hawaii from the Philippines (13), and a frugivorous
bat (Vampyressa pusilla) evidently boarded a vessel passing
through the Panama Canal and was later found aboard when the
ship was between Australia and Tasmania (14).

Translocation after Using Ships for Shelter
Bats sometimes roost in or on ships in port and may be
transported as a consequence. Silver-haired bats were discovered
hibernating in hulls of ships, and numbers of them found
various refuges on ships and yachts in New York (15). Little
Brown Bats (Myotis lucifugus) roosted aboard a ship that frequently
traveled from Canada to Europe, flying ashore after
arrival in the Netherlands and England (16). The presence of
individual Little Brown Bats in rabies-free Iceland (9) and
Kamchatka, Russia (17), has been attributed to travel by ship.
RABV, other viruses, and Histoplasma capsulatum have been
found in this species (3,8).
On January 21, 1997, a stevedore working in the hold of a
ship being unloaded in Long Beach, California, after its arrival
from Korea, was bitten on the back of his neck by a bat. A fluorescent
rabies antibody test was negative for RABV infection.
On February 1, I received the bat for evaluation and determined
it to be a Serotine bat (Eptesicus serotinus), which is similar to
the Big Brown Bat (E. fuscus) but with a slightly more massive 
skull. The Serotine has been reported in North Africa and
England and across Europe and Asia to Korea. Hundreds of ill
or dead Serotines have been found infected with the
RABV-related European bat lyssavirus 1 (EBLV-1) in Europe,
where one or two persons have died of the infection after bat
bites (5). The rabies conjugate used in the rabies test on the
Serotine bat’s brain reportedly reacts with this virus as well.

Translocation in Shipping Containers

Translocation of bats by ship also occurs when bats are
closed inside shipping containers. Free-tailed bats from the
tropics are occasionally transported long distances in fruit
shipments (18). A Pallid Bat (Antrozous pallidus) was discovered
in Victoria, British Columbia, in a shipment of lettuce
from California (19), where RABV-infected Pallid Bats have
been identified. A Big Brown Bat was found hibernating in a
timber container from Canada when it was unloaded in the
Netherlands (16). An Asiatic Pipistrelle bat (Pipistrellus javanicus)
was discovered in a container transported by ship from
Japan to New Zealand (20). Sasaki et al. (21) reported the
arrival in rabies-free Hawaii of a RABV-infected Big Brown
Bat found flying in an automobile container from California.
Subsequent study indicated that previously the bat had been
transported to California either from Florida in the shipping
container or from Michigan in an automobile.
In October 1995, a group of live bats was observed hanging
in a dark corner within a large shipping container that had
just arrived at a Los Angeles port from Puerto Rico, but the
bats escaped as capture was attempted and no further reports
of these bats were made. Histoplasmosis, apparently absent in
California except for imported human infections, has been
diagnosed in some Puerto Rican bats.

Translocation by Aircraft

Bat translocation by aircraft has been reported several
times. A Little Brown Bat was found clinging to a seat in an
airplane at the end of a flight in Canada (22). An Eastern Pipistrelle
bat (Pipistrellus subflavus) was recovered from a plane
that had just arrived in Texas from Mexico (23); RABVinfected
bats of this species have been identified in the United
States and Canada. The carcass of a Little Brown Bat, presumably
from Tacoma, Washington, was found on a runway at an
Air Force base on rabies-free Guam (24). Stebbings reported
the arrival in England of a Silver-haired Bat aboard a U.S. Air
Force cargo plane from Delaware (25). Observed flying in the
plane en route, the bat was captured later while sleeping in a
crew member’s bed in the aircraft.
An Asiatic Pipistrelle bat was captured May 25, 1993,
aboard an airliner en route from Tokyo to San Francisco. This
bat was negative for RABV. The next month a Yuma Myotis
bat (Myotis yumanensis) was discovered flying aboard a U.S.
Air Force cargo plane en route from California to Hawaii. This
bat was also negative for RABV, although rabies has been
diagnosed in the species in California. Evidently the bat was
loaded into the aircraft within a shipment of fruit.
In early March 1995, a traveler who had just arrived in Los
Angeles by aircraft from South Africa opened his suitcase and
observed a bat fly out. The suitcase had been closed three days
earlier during darkness in a hut within Kruger National Park.
The bat was negative for RABV, and the frozen carcass was
sent to me 2 months later with the history of origin in a Los
Angeles County community. At first glance, the bat appeared
to be a common local free-tailed bat (Tadarida brasiliensis),
but closer inspection indicated differences, although the bat
belonged to a family with similar representatives in warm
areas worldwide. After extensive study, I determined the specimen
to be a Wrinkle-lipped bat (Chaerephon pumila), known
throughout sub-Saharan Africa, Madagascar, and southern
Arabia. Further research disclosed the transported bat’s African
origin. This species supports experimental replication of
Ebola virus without showing disease signs (26); the remainder
of the carcass was immediately sent to a federal laboratory for
Ebola virus tests, which proved negative. Several other viruses
have also been isolated from the salivary glands of this species
in Africa (3).
In June 1997, a woman was bitten by a bat hiding in clothing
she was packing before an airline flight from Costa Rica to
California. The live bat was restrained in a plastic bag during
the flight; it was dead on arrival. The bat was negative for
RABV and was identified as a Sinaloan Mastiff Bat (Molossus
sinaloae), an insectivorous species in which RABV has been
reported (5).

Translocation for Confinement

Bats have been transported varying distances, sometimes
worldwide, to be maintained in captivity as research animals,
as live specimens in zoos or other exhibits, and as pets. Transport
for research purposes is not noteworthy except in unusual
circumstances. A Big Brown Bat in the incubational stages of
rabies was among live bats sent from Canada to a laboratory in
Germany, where the bat developed clinical rabies (27). Similarly,
six Big Brown Bats that were incubating RABV were in
a group sent from the United States to a laboratory in Denmark
(28). However, recipient laboratories understood the risks and
had taken necessary precautions.
RABV-infected individual bats of the tropical American
common Vampire Bat (Desmodus rotundus) have been
reported throughout their geographic range, which extends
from northern Mexico south to Chile and Uruguay (8,29).
RABV has also developed in Vampire Bats after being transported
to laboratories. In addition, during the 1970s, a group of
these bats sent from Mexico to a laboratory in the United
States presumably escaped en route, because only the empty
shipping container arrived.
Increasing interest in bats has resulted in displaying of
more varieties of these mammals, including Vampire Bats, to
the public (5). One such display presented a problem I investigated
in 1988 after four of eight Vampire Bats escaped their
flight cage within a cavelike structure at a southern California
zoo 1 month after their arrival from Mexico through a Texas
Emerging Infectious Diseases • Vol. 9, No. 1, January 2003 19
supplier. Two escaped bats were found dead, possibly due to
starvation or unusually cold weather. One dead bat had nearly
escaped the building, and the other was outside. Neither bat
was infected with RABV. The apparent escape route to the outside
was through a fragile false cave ceiling, which could not
be inspected. This ceiling may have contained the carcasses of
the remaining two missing bats, possibly a male and a female.
I found no bat bites on zoo animals and no bats or bat feces in
likely hideaways in the zoo.
The large fruit-eating bats (genus Pteropus) live on land
masses, including islands, from Madagascar, India, Southeast
Asia, the East Indies, the Philippines, and Australia to the
Samoan and Cook Islands of the South Pacific Ocean. They
have been popular zoo attractions for many years. RABV was
reported in a Pteropus in India (8), and RABV-related lyssaviruses
were reported in four species of Pteropus and an insectivorous
species in Australia, where two persons died of these
infections (30).
Three additional viruses (Paramyxoviridae family)
ascribed to Pteropus origin have proven pathogenic or fatal to
people and domestic animals. Four species of Australian
Pteropus bats in Queensland carry Hendra virus without developing
symptoms. These bats disseminate virus in urine or placental
fluid during birthing, and the virus is later ingested by
pregnant horses that amplify the virus, which then spreads to
people and causes a fatal pneumonia (13/20 horses were
infected in a 1994 outbreak, which resulted in two human
deaths) (30). The second virus, Menangle virus, is considered
to be spread to pigs in Australia by the same four species of
Pteropus bats, producing stillbirths with deformities in 1998 in
27% of litters, as well as an influenzalike illness in humans
(30). The third virus, Nipah virus, identified in urine and saliva
of Pteropus bats in Malaysia, apparently spreads the virus to
pigs and destroyed that country’s swine industry in 1998. The
virus spread from pigs to hundreds of industry workers;
approximately 40% of these workers died of severe viral
encephalitis caused by the agent (31).
Importation of fruit-eating bats has long been severely
restricted to protect the fruit industry in the United States. The
Egyptian Rousette bat (Rousettus egyptiacus) is a widespread
Old World fruit bat that readily reproduces in captivity; thus
colonies occur in some zoos. This species has been implicated
in several viral infections in Africa (3). An error occurred in
1994, when thousands of these and other bat species were permitted
entry into the United States for sale as pets or for exhibition
(28); this procedural mistake resulted in a policy change
to prevent recurrence. Antibodies to West Nile virus (WNV)
had been reported in the R. egyptiacus species in Uganda and
Israel (3), and the virus had been isolated in India from the
nearly indistinguishable R. leschenaulti, which overlaps geographically
with R. egyptiacus in Pakistan (32). The entry of
R. egyptiacus into the United States in 1994 suggests a remote
connection with the subsequent outbreak of WNV there, first
observed 5 years later among captive and wild birds at a zoo in
New York (33).
In 1997, two R. egyptiacus bats died with rabies-like
symptoms in a Denmark zoo; they were later found to be
infected with EBLV-1 subtype A, a RABV-related agent
known to have caused deaths in European insectivorous bats
and in humans. The two infected bats had arrived recently
from a Netherlands zoo, where the source captive bat population
subsequently was destroyed (34). A replacement colony
was similarly destroyed after a bat originating from a Belgian
zoo was also determined to be infected (35).
Persons concerned about sick and injured wildlife often try
to rehabilitate disabled bats, sometimes transporting the animals
a considerable distance from sites of discovery. Unfortunately,
an average of 10% of disabled bats tested in North
America are found to be infected with RABV, exposing those
trying to rehabilitate the bats to rabies. If they have received
preexposure rabies prophylaxis in advance, these persons are
advised to take booster shots of vaccine; otherwise, they are
advised to take both antirabies globulin as well as the full vaccine
Often, attempting to reverse the negative image of bats
usually held by the public, persons trying to rehabilitate sick
bats may suppress warnings of rabies hazards, doing both bats
and the public a disservice. Moreover, to avoid the embarrassment
of repeated exposures to rabid bats, some persons working
in bat rehabilitation are known to arrange submission of
rabies-suspect bats to a variety of different laboratories in different
geographic areas, thus disguising the true history of the
bat; this practice may protect the rehabilitator but prevent
other persons or pets exposed earlier from receiving adequate
antirabies management.

Translocation for Release

Bats have been translocated and released in attempts to
establish bat populations in new areas for reasons such as insect
control and experimental study. Such efforts are sometimes
supplemented by providing living quarters or shelters for bats
ranging from elevated boxlike structures to tunnels. Before the
knowledge that some insectivorous bats might be infected with
rabies or other pathogens, bats were sometimes transported
great distances over land or overseas and released in efforts to
establish populations at the new location. Tomich (13) assembled
historical records about the importation and release in
rabies-free Hawaii of Asiatic Pipistrelle bats from Japan and
free-tailed bats (Tadarida brasiliensis) from California during
the late 1800s to establish bat populations for insect control
purposes, but the attempts were evidently unsuccessful.
Observing that destruction of old-growth forests eliminated
the tree hollow homes of Polish bats, Krzanowski (36)
recommended the introduction into Poland of Red Bats and
Hoary Bats from the United States because these species take
shelter in tree foliage rather than hollows, and they migrate at
the approach of cold weather rather than hibernate in tree cavities.
However, rabies was discovered simultaneously in North
American insectivorous bats, including these two species, discouraging
further consideration of the proposal.

20 Emerging Infectious Diseases • Vol. 9, No. 1, January 2003
The homing abilities of bats have routinely been studied by
transporting and releasing marked bats up to 805 km from
their home roost, which is then monitored for the return of the
marked bats (37). RABV infection has now been identified in
11 of the 12 North American species studied, and histoplasmosis
is known in 6; RABV-related lyssavirus infections have
been reported in 5 of 12 European species studied (8).
During World War II, field trials were conducted in the
southwestern United States to determine the effectiveness of
disseminating thousands of free-tailed bats (T. brasiliensis) in
the air, each transporting a small time-activated fire bomb. The
objective was to start thousands of simultaneous fires in adversary
target areas, achieved after each bat had sought out a hideaway
in various available structures (38). As a participant in
the project, I observed that each bomb or dummy bomb,
attached by a short string and surgical clip to the bat’s abdominal
skin, was disengaged after the bat alighted in a refuge and
chewed through the string. Thousands of bats were transported
<1,609 km distant from source bat caves in Texas and New
Mexico to test areas in California, New Mexico, and Utah.
Frequently, the tests were postponed, and the freshly captured
bats were released unencumbered at or near test sites.
Unknown at the time, RABV is now known to occur in 0.5%
of bats in the source caves (8), so the virus was almost certainly
translocated with the bats. H. capsulatum, the causative
fungus of histoplasmosis, also has been isolated from these
bats and their guano in the source caves, but neither bats nor
guano have yielded the agent in extensive surveys in California,
which is regarded as free of the fungus; no cases of indigenous
origin have been detected (8).

Bats and the pathogenic organisms they sometimes harbor
are being transported by humans within and between continents,
and sometimes these transported bats escape. Because
bats reproduce slowly (usually only one or two offspring are
produced annually by a female), the chances of successful
introduction of the species are minimized. Populations would
more likely develop should large numbers be freed in places
favorable to survival. Although a single escaped bat might not
survive long or reproduce, it would seek shelter in places frequented
by local bats to which it might transmit pathogens. As
has been observed, introduced pathogens include RABV, other
lyssaviruses, or various other agents.
Vampire Bats can be especially problematic in view of
their possible colonization in warm climates and their dependence
on a diet of blood, thus necessitating their biting vertebrates,
including man and domestic animals. As reported, in
addition to their known role as biologic vectors of rabies to
humans and domestic animals and surra (Trypanosoma evansi)
to horses and cattle, Vampire Bats can also be temporary biologic
as well as mechanical vectors of Venezuelan equine
encephalomyelitis virus and foot-and-mouth disease. They are
likely effective mechanical vectors if not biologic vectors of
any bloodborne pathogen, including the AIDS virus (29). Various
species of fruit-eating bats are infected at times with
pathogens destructive to other bats, humans, and domestic animals.
However, their entry to many areas is restricted due to
concern that their escape would lead to populations destructive
to fruit crops.
Accidental or planned translocations of bats between land
masses happens almost certainly with far greater frequency
than is reported. Such events can be embarrassing, and
although incidents that result in successful containment are
more likely to be reported, failed efforts can remain unpublicized.
Relevant reporting requirements do not exist. Personnel
involved in the various described incidents generally have performed
very well in efforts to resolve the problems, often with
immediately contrived solutions. Inspectors at entry centers
are usually exceptionally competent because they must cover a
broad array of subject areas, but their competency must be
taxed at times. For example, most bats are exceptionally adept
at avoiding capture, and even bat scientists with special equipment
frequently are outmaneuvered. Some inspectors contact
specialists for help in emergencies, but help is not always
available or is displaced by previous commitments and economic
necessities. Previous contractual arrangements with
institutions such as universities, natural history museums,
zoos, or specialized commercial services could dispel most relevant
problems, including funding, and maintain program continuity.
Unaffiliated specialized personnel would be expected
to maintain or acquire relevant competency, but incidents,
such as those cited here, show some lapses. Ideally, the services
of a bat expert are required. For example, if bats are to be
excluded from any vehicle of conveyance, the usual procedures
and equipment should be reviewed by responsible persons
very familiar with bats, their capabilities, their capture,
their confinement, and their exclusion in order to recognize
flaws that permit bats to be transported. Thus, experts can help
establish and maintain more effective programs.

Appreciation is extended to the counties and state of California
and to William E. Rainey, Elizabeth D. Pierson, Charles E. Rupprecht,
Jean S. Smith, Kevin F. Reilly, Thomas H. Kunz, and Amy Turmelle
whose help made relevant reports possible.
After the 1953 discovery of bat rabies in the United States, Dr.
Constantine established the Southwest Rabies Investigations Station
in New Mexico for the Centers for Disease Control and Prevention
and developed its program to investigate the problem and control bat
rabies. Now retired, he continues research in the field.

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Address for correspondence: Denny G. Constantine, 1899 Olmo Way, Walnut
Creek, California, 94598 USA