Vampire bat-transmitted rabies in cattle
Biology, ecology and control of the vampire bat
C. Arellano Sota
The author is FAO Regional Animal Production and Health Officer for Latin America and the Caribbean, Santiago, Chile.
Rabies transmitted by vampire bats has existed in tropical America since the pre-Hispanic era. Originally the epidemiological cycle of the disease involved mainly wildlife, with the vampire bat being the main vector of the disease and the wild mammals of the region its victims.
With the arrival of domestic mammals and with the European conquest and colonization, the vampire bat changed its feeding habits, preferring to feed on domestic mammals, especially cattle. Since the vampire bat is a very effective vector of the rabies virus, vampire-transmitted rabies became a very important limiting factor for the development of livestock production in most countries of Latin America and the Caribbean.
In 1968, the National Institute for Livestock Research in Mexico established a cooperative programme to create and evaluate the technology needed to control vampire bat rabies. The programme was set up with the collaboration of FAO and the Fish and Wildlife Office of the United States and was financed by the Mexican Government, the United Nations Development Programme (UNDP) and the United States Agency for International Development (USAID).
History
As previously stated, vampire-transmitted rabies has probably existed in tropical America since the pre-Hispanic era. Several authors have referred to this problem: Fernandez de Oviedo, in his book Sumario de la Historia Natural de las Indias, mentioned that many soldiers died from bat bites during the Darien conquest and Molina Solis, in Historia del Descubrimiento y Conquista de Yucatán, mentioned that many soldiers and horses of Francesco de Montejo's army were attacked by vampire bats.
The first scientific report concerning bovine rabies in tropical America was by Carini in 1911, in São Paulo, Brazil (Carini, 1913). He observed Negri bodies in a bovine brain and was able to produce paralytic rabies in rabbits with this material. In 1931, Pawan first isolated the rabies virus from different species of bats, including Desmodus rotundus, the common vampire bat (Pawan, 1936). In 1931, Telles Girón in Mexico demonstrated that derringue, the fatal paralytic disease in cattle, was caused by the rabies virus (Telles Girón, 1945). In the following years, several scientists reported the disease in Colombia, Venezuela, Central America and Panama. We know now that paralytic bovine rabies from vampire bites only occurs in the Americas in areas 1 800 to 2 000 m above sea level and at latitudes between 33°S and 28°N. The important limiting factor for vampire bats is the winter temperature; they cannot live in areas where the temperature drops below 15°C (Ache, 1968).
Epidemiology
Acha (1968) published an epidemiological study on paralytic bovine rabies in the Americas. This very important work showed the disease as it was before the new tissue culture vaccines for bovine rabies were used in the field and before effective methods for vampire control became available. Table 1 shows that, in 1968, bovine paralytic rabies killed 512 500 head of cattle; the cost of damages was approximately US$47 529 000.
At the end of the 1960s, the problem of bovine paralytic rabies was already well known. However, the technology was not yet available to control vampire bat populations, the most important vector of the disease, and most existing vaccines did not provide good protection for cattle.
Vaccines
Only tour commercial Flury high egg passage (HEP) vaccines were capable of protecting 28 to 70 percent of the vaccinated cattle when they were challenged with a known, lethal vampire virus (Arellano, 1980).
Atanasiu et al. (1968) evaluated the efficacy of six bovine vaccines by measuring antibody production. He demonstrated that five of the vaccines induced circulated antibodies that were still present one year after vaccination in more than 50 percent of the vaccinated cattle (Table 2).
Several vaccines were tested between 1971 and 1976 at the National Institute of Livestock Research in Mexico. The efficacy of a vaccine was measured by challenging with a known strain of rabies virus of vampire origin; more than 80 percent protection was noted one year after vaccination with six of the seven vaccines evaluated, and 100 percent protection was noted three years after vaccination with three of the seven vaccines (Table 3) (Arellano, 1980; Hernández, 1976; Batalla et al., 1971).
Since the mid-1970s, there have been effective vaccines and the technology has been available for the reduction of bovine paralytic rabies in the tropical regions of the Americas. However, success has not been achieved, as we can observe from Table 4.
Conclusions
Of the 18 countries affected by bovine paralytic rabies, seven have been able to reduce their problems; seven have maintained their epidemiological situation as it was in 1968; and four have seen their problems increase. Applied research has demonstrated that there are vaccines available for protecting cattle against rabies and that there are also selective and effective methods of reducing vampire bat populations (e.g. the application of anticoagulants such as diphenadione and warfarin). Nevertheless, this technology has not been properly transferred through the veterinary services of the affected countries, with the exceptions of Bolivia, Brazil, Guatemala, Mexico, Nicaragua, Panama and Paraguay, which have reported reductions in the problem (FAO/OIE/WHO, 1969; 1979; 1986).
The information in the Animal Health Yearbooks (FAO/DIE/WHO, 1969; 1979; 1986) is more qualitative than quantitative, but it allows us to observe that some countries have been successful in reducing the rabies problem. In any case, throughout the affected region efforts should be made to make easily available both the anticoagulant products for the reduction of the vampire bat population and the rabies vaccines which, when handled properly, have proved effective in cattle.
The bat is the only flying mammal, a characteristic referred to in the word for "bat" in many languages: Fledermaus (German), fleder-mus (Swedish), flager-mur (Danish) and sorits-pennada (Provençal); they all mean a mouse or rat with wings. In Chinese, the word for "bat" is sein-shii (celestial mouse), and in Nahuatl, a language used by the Aztecs in central Mexico, the word was quimich-papalotl (butterfly-mouse).
In this discussion we will refer specifically to the blood-lapping, haematophagous bat. Buffon was the first to call this bat "vampire", a name of Slavonic origin, referring to a ghost that supposedly sucked blood from its victims.
Biology of the haematophagous bat
Taxonomy. The order of Chiroptera (from cheiros hand, and pteron wing, i.e. animals with hands turned into wings) is divided into two suborders: Megachiroptera and Microchiroptera. The Megachiroptera are the big fruit-eating bats known as flying foxes. These are found only on the South Sea islands - principally Java and the Philippines - and also in Madagascar. The Microchiroptera are distributed worldwide, including areas occupied by the Megachiroptera. Of note is that only three of the more than 90 Microchiroptera species are haematophagous, and these are found only in the Americas. Taxonomically, they belong to the Phyllostomatidae family, Desmodontidae subfamily, with only three genera: Desmodus, Diphylla and Diaemus. The three have only one species each: Desmodus rotundus, Diphylla ecaudata and Diaemus youngi (Flores-Crespo and Arellano-Sota, 1988).
Anatomic characteristics. Villa-Ramírez (1976) describes the anatomic characteristics of the haematophagous bat as follows: length of head and body, <90 mm; hair with several tones of brown; a short skull of conical shape; open nostrils on the surface of a reduced nasal leaf; a short interfemoral membrane, without tail; a long thumb with two pads in the genus Desmodus, a shorter thumb in Diphylla and an even shorter thumb in Diaemus; long leg bones: and wings that accommodate the muscles. According to Anderson and Knox (1967), the dental formulas for the three genera are as follows: Diphylla, 2/2, 1/1, 1/2, 2/2 = 26; Diaemus, 1/2, 1/1, 1/2, 2/1 = 22; Desmodus, 1/2, 1/2, 2/3, 0/0 = 20.
1. Bovine paralytic rabies in the tropical Americas in 1968
Rage paralytique bovine dans les tropiques américains, 1968
Rabia paralítica de bovinos en América tropical durante 1968
|
Country |
Number of outbreaks/year |
Estimated number of bovine deaths from rabies |
|
Argentina |
18 000 |
50 000 |
|
Brazil |
32 200 |
200 000 |
|
Bolivia |
20 000 |
50 000 |
|
Belize |
815 |
2 000 |
|
Cayenne |
600 |
1 000 |
|
Costa Rica |
132 |
10 000 |
|
Colombia |
5 300 |
50 000 |
|
Ecuador |
930 |
5 000 |
|
El Salvador |
1 080 |
3 000 |
|
Guatemala |
1 120 |
12 000 |
|
Guyana |
2 000 |
3 000 |
|
Honduras |
348 |
6 000 |
|
Mexico |
1 502 |
90 000 |
|
Nicaragua |
831 |
10 000 |
|
Panama |
218 |
8 000 |
|
Paraguay |
320 |
5 000 |
|
Suriname |
733 |
2 000 |
|
Trinidad/Tobago |
2 |
500 |
|
Venezuela |
215 |
5 000 |
|
Total |
86 346 |
512 500 |
Source: Acha, 1968.
2. Efficacy of rabies vaccines, evaluated by the titre of neutralizing antibodies in bovines
Efficacité des vaccine contre la rage, évaluée sur la base des anticorps neutralisants chez les bovine
Eficacia de la vacuna antirrábica evaluada en función de la presencia de anticuerpos neutralizantes en ganado bovino
|
Vaccine |
Total vaccinated |
Number with neutralizing antibodies after 365 days (%) |
Median titre of neutralizing antibodies at 365 days |
|
ERA strain in pig kidney cells |
8 |
2 (87.5) |
24 |
|
HEP strain in chicken embryo |
20 |
11 (55) |
2 |
|
HEP strain in chicken embryo and Al(OH)3 |
8 |
2 (25) |
<2 |
|
HEP strain in dog kidney cells |
10 |
0 (0) |
<2* |
|
Fixed virus strain in suckling mouse brain |
6 |
6 (100) |
6 |
|
Fixed virus strain in suckling mouse brain and Al(OH)3 |
10 |
9 (90) |
27 |
Note: ERA = Evelyn-Rokitnicki-Abelseth; HEP = high egg passage.
* 200 days.
Source: Atanasiu et al., 1968.
3. Duration of immunity and protection1 in bovines given different antirabies vaccines
Durée de l'immunité et de la protection chez les bovins auxquels ont été administrés différents vaccine contre la rage
Persistencia de la inmunidad y protección de bovinos tratados con diversas vacunas antirrábicas
|
Vaccine |
Duration of immunity (months) |
Percentage of animals protected |
|
ERA strain in pig kidney cells |
72 |
100 |
|
V.319 (Acatlán) strain in BHK cells² |
33 |
100 |
|
|
45 |
87 |
|
Pitman Moore strain in Nil II cells (inactivated) |
36 |
100 |
|
Roxane strain in pig kidney cells |
12 |
100 |
|
IB strains in pig kidney cells |
12 |
80 |
|
Flury (HEP) strain in dog kidney cells |
6 |
20 |
Note: ERA = Evelyn-Rokitnicki-Abelseth; HEP = high egg passage.
1 Demonstrated by viral challenge.
² There were two trials of this vaccine.
Source: Arellano, 1980.
4. Changes in the incidence of bovine rabies from 1968 to 1985
Variations de l'incidence de la rage bovine de 1968 à 1985
Cambios en la incidencia de la rabia en bovinos, entre 1968 a 1985
|
Coventry |
1968 |
1978 |
1985 |
Overall result |
|
Argentina |
C |
C |
L |
I |
|
Brazil |
H |
H |
M |
R |
|
Bolivia |
H |
H |
M |
R |
|
Belize |
... |
L |
L |
S |
|
Costa Rica |
C |
C |
L |
I |
|
Colombia |
C |
C |
C |
S |
|
Ecuador |
L |
L |
L |
S |
|
El Salvador |
L |
M |
H |
I |
|
Guatemala |
C |
M |
L |
R |
|
Guyana |
C |
M |
M |
S |
|
Honduras |
C |
L |
L |
S |
|
Mexico |
C |
H |
M |
R |
|
Nicaragua |
H |
L |
L |
R |
|
Panama |
H |
L |
M |
R |
|
Paraguay |
M |
C |
C |
R |
|
Suriname |
U |
L |
L |
S |
|
Trinidad/Tobago |
L |
L |
L |
S |
|
Venezuela |
C |
C |
L |
I |
Note: U = unlikely to be present; C = confined to certain regions; L = low sporadic incidence; S = same situation since 1968: M = moderate incidence; R = reduction of incidence since 1968; H = high incidence; I = increase of incidence since 1968.
Source: FAO/OIE/WHO (1969, 1979, 1986).
5. Effectiveness of anticoagulants in reducing vampire bat populations
Efficacité des anticoagulants dans la réduction des populations de vampires
Efectividad de anticoagulantes en la disminución de la población de murciélagos vampiros
|
Method |
Percentage reduction in number of bites |
Reference | |
|
Topical treatment of vampires |
95.0 |
Flores-Crespo, Burns and Said (1974); | |
|
Treatment of vampire niches |
60.0-90.0 |
Flores-Crespo, Ibarra and De Anda (1976) | |
|
Topical treatment of bites on victim |
81.1-94.9 |
Flores-Crespo, Ibarra and De Anda (1976); | |
|
Systemic treatment of cattle: |
|
| |
|
|
- Intraruminal (diphenadione) |
93.0-97.8 |
Thompson, Mitchell and Burns (1971) |
|
|
- Intramuscular (warfarin) |
87.5-96.4 |
Flores-Crespo, Ibarra and De Anda (1976) |
Ecology of the vampire bat
Antiquity and distribution. There is no evidence of the existence of vampire bats anywhere other than in the Americas. Fossil evidence indicates that vampires bats have been in the Americas since the Pleistocene period approximately 2.5 million years ago (Gut, 1959; Koopan, 1958). The present distribution of the haematophagous bat covers almost all of Latin America, including tropical, subtropical and even some temperate zones from the Tropic of Cancer in Mexico to the Tropic of Capricorn in Argentina and Chile. These bats are definitely tropical animals.
Of the three genera, Desmodus is the most widely distributed and is most abundant in Mexico and Central and South America. Diphylla comes second in distribution and in number of colonies; it is encountered most frequently in the Amazon region but is also found in southern Brazil, Mexico and Peru (Cabrera, 1957). Diaemus has more or less the same distribution as Diphylla, but it is considered a very rare species with a limited number of colonies; the number of specimens collected has been very low (Pawan, 1936).
Feeding habits. Blood is the only food taken by the vampire bat. The bat is equipped with sharp incisor teeth which cut the skin of victims. Two channels on each side of the bottom of the tongue permit the bat to lap blood. The morphology of the gastrointestinal tract has been described by several authors (Grasso, 1955; Park and Hall, 1951).
The attack pattern of Desmodus on bovines has been studied in Mexico with the use of night-viewing equipment. Vampire bats are capable of biting any part of the body of cattle. However, bites are more frequent on the neck, ears and around the base of the tail (Flores-Crespo et al., 1974). Campos-Vela (1972) demonstrated that more than 90 percent of the vampire bats captured in different regions of Mexico had fed on domestic livestock.
Habitat and behaviour. There are a great variety of refuges and roosts for vampire bats: caves, house roofs, abandoned mines, tunnels, hollow trees, wells and so forth. All are suitable if the average temperature is from 21° to 28°C and the relative humidity is less than 45 percent (Flores-Crespo and Arellano-Sota, 1988).
The number of individuals in a colony may vary from less than ten to 300. Although most colonies are in this range, rare colonies with more than 2 000 individuals have been found in Mexico and Brazil (Flores-Crespo and Arellano-Sota, 1988). The number of individuals in a colony appears to depend on the availability of food, space and suitable climatic conditions. Studies of banded vampire bats showed that there is some interchange of individuals among refuges, but the population of a colony generally remains stable (Villa-Ramírez, 1966; Wimsatt, 1969; Lopez-Forment, Schmidt and Greenhall, 1971).
Vampire bat - Vampire - Murciélago vampiro
The use of radiotelemetry confirmed the idea that a vampire bat may use several refuges (Mitchell, Burns and Kolz, 1973). Other studies showed that banded vampire bats were found in the refuges where they had originally been banded seven years (Flores-Crespo et al., 1976) and 12 years earlier (Málaga, 1959). These studies show that vampire bats can use different refuges but that they are always within their area of activity - an area of 10 to 20 km².
Moonlight influences the foraging behaviour of the haematophagous bat. Several studies have clearly demonstrated that there is practically no vampire foraging activity when the moon is out (Flores-Crespo et al., 1976).
Reproduction in Desmodus sp. has been extensively studied. These bats have several oestrus periods a year. The gestation period is about five months and, with few exceptions, only one offspring is born. The mother takes care of the young for almost one year.
Together but never mixed. The results of more than 200 observations indicated that refuges are shared by several bat species, but that each species has its own territory. The haematophagous bat was never found mixed with other bat species. It was also observed that vampire bats remained clustered in their niche, maintaining close contact with all individuals in the colony (Flores-Crespo and Arellano-Sota, 1988).
Cleaning habits. A study of the behaviour of the vampire bat in captivity, using a closed-circuit television system, revealed that the bats use their tongues and feet to clean their bodies. During a six-hour observation period, it was noted that the vampire bats spent an average of 34 minutes cleaning themselves and had an average of 260 mouth-body contacts. These observations strongly suggested that any substance that could be spread over the skin would be ingested by the vampire bat (Flores-Crespo, Linhart and Burns, 1972).
Feeding on cattle. The feeding patterns of vampire bats on cattle were studied with the use of night-viewing equipment under laboratory conditions in a closed corral. A total of 49 biting incidents were observed; 27 bites were on the interdigital region of cattle that were standing and 22 were on various parts of the body of cattle that were lying down. Only one animal was bitten on the back. There was very little contact between the vampire bat and its victim (Flores-Crespo, Linhart and Burns, 1971).
With the use of night-viewing equipment under field conditions, it was demonstrated that the Holstein breed was bitten significantly more than the Brahman or the Charolais breed. The difference appears to be related to the temperament of the animals; tamer cattle are bitten more often. It was also observed that vampire bats preferred to bite animals that were lying down. Nevertheless, they were capable of biting different parts of the body, including the neck and legs, while the victim was standing (Flores-Crespo et al., 1974).
Control of the vampire bat
Other wild or domestic vectors of rabies normally bite only when they are disturbed, but the members of the Desmodontidae have blood-lapping habits and must bite to feed. Therefore, when rabid, these bats are the most effective rabies vectors. They are by far the most frequent cause of outbreaks of rabies in livestock in Latin America and some Caribbean countries. In 1959, Málaga reported that there were annual losses of one million head of cattle in Latin America as a result of paralytic rabies and, in 1968, Acha estimated the doss to be 0.5 million (Málaga, 1959; Acha, 1968).
There is, then, ample justification for all the efforts that have been made to control vampire bats in Latin America. Cattle owners have long demonstrated an interest in using different methods to fight the vampire bat. These techniques were based on observations of vampire bat behaviour; they were effective up to a certain point, but most had limitations. Some techniques were not practical, some were expensive and others could disturb the ecology of other bat populations or even be toxic for humans. Among the more common techniques were the use of lighting in corrals; chicken-wire to protect corrals; smoke and fire in the refuge; toxaphene and diesel fuel in the refuges; and explosives in caves; as well as the application of poisonous substances in old bite wounds and the setting of traps and nets (Flores-Crespo, 1978).
Agents for the control of haematophagous bats. Several aspects of the behaviour of vampire bats as well as results of experiments have led us to believe that good results can be obtained with the use of slow-acting chemical anticoagulants such as chlorophacinone (2-[(p-chlorophenyl) phenylacetyl]-1,3-indandione), siphenadione ((2-diphenylacetyl)-1H-indene-1,3 (2H)-dione) and warfarin (3-(-acetonylbenzyl)-4-hydroxycoumarin). Warfarin was cheaper, more easily available and equally effective (Said, 1973).
Topical treatment of the vampire bats. This method of control is based on studies of the preening habits of vampire bats and on the fact that haematophagous bats live together with other kinds of bats but never mix with them (Flores-Crespo, Linhart and Burns, 1972). The method consists of capturing a small number of haematophagous bats with mist-nets spread around corrals, with bitten cattle used as bait. Anticoagulant in a petrolatum base is applied to the skin of the captured vampire bats and they are then released to return to their refuges where they contaminate their mates. Later, when they preen themselves by licking their skin, they ingest the anticoagulant and die (Flores-Crespo, Burns and Said, 1974; Flores-Crespo and Said, 1972). The results of this method and others are shown in Table 5.
This technique has been demonstrated to be selective; it does not affect any other species of bat. Vampire bat populations are effectively reduced, as was shown in campaigns carried out in Brazil, Colombia and Mexico.
Treatment of the vampire niches. Another method of eliminating vampire bats is to apply an anticoagulant to the surface of niches inside the refuges where vampires rest. The animals come into contact with the substance and ingest it during their cleaning activity. Chlorophacinone (Flores-Crespo, Burns and Said, 1974), diphenadione (Flores-Crespo and Said, 1972) and warfarin (Flores-Crespo, Ibarra and De Anda, 1976) have been tested with this procedure and were found to be 90 to 100 percent effective in the treated colonies. Six months after treatment, the niches were not repopulated and no harm was done to any of the other species of bats that were living in the same refuge. In one case (Flores-Crespo and Said, 1972) it was observed that the dead vampires were eaten by terrestrial mammals with no resultant toxic effect. This is attributable to the fact that vampire bats are very susceptible to anticoagulants and the amount of active substance in the compound is consequently very low (0.91 mg/kg for warfarin and diphenadione).
This method is considered to be effective but is not always practical because it is difficult to find vampire bat refuges and sometimes their niches cannot be reached.
Topical treatment of bite wounds. Generally, haematophagous bats remove the scars of old wounds instead of making new injuries. Thus, it is possible to apply an anticoagulant compound to bites made by the vampire bats on cattle. This method proved to be 100 percent effective under experimental conditions. Under field conditions at three different ranches, this method resulted in an 81.1 to 94.9 percent reduction in the number of bites 15 days after treatment (Flores-Crespo, Ibarra and De Anda, 1976). The method is selective and effective but has the disadvantage that one must have contact with bitten animals every time the anticoagulant is applied.
Systemic treatment of cattle. This method consists of producing levels of anticoagulant in cattle blood that are not high enough to cause coagulation problems in the treated animal but that are sufficient to last several days and kill the vampire bats that feed on the cattle.
The first treatment of cattle with an anticoagulant was developed by Thompson, Mitchell and Burns (1971), who administered a 0.05 percent suspension of diphenadione by the intraruminal route. Under laboratory conditions, this was 100 percent effective at 24,48 and 72 hours after administration and was 33 percent effective after 96 hours (Thompson, Mitchell and Burns, 1971).
The second systemic administration of an anticoagulant was developed by Flores-Crespo et al. (1979), who injected cattle intramuscularly with 5 mg of soluble warfarin/kg. This method is more commonly used and is much better known than the intraruminal method. Under laboratory conditions this treatment was 100 percent effective at 24, 48, 72 and 96 hours after administration and was 50 percent effective after 120 hours.
In field conditions this technique was evaluated in four ranches located in two different regions in Mexico Yucatán and San Luis Potosí. The number of bat bites in cattle 11 to 12 days after administration was reduced by 87 to 96.4 percent.
Pharmacological and toxicological studies of diphenadione, administered intraruminally (Thompson, Mitchell and Burns, 1971; Flores-Crespo et al., 1979; Bullard, Thompson and Holguin, 1976), and warfarin, administered intramuscularly (Flores-Crespo, Linhart and Burns, 1971; Flores-Crespo et al., 1979; Amaya and Carrera, 1976), showed that there were no adverse effects in cattle.
Conclusions
The results of these studies demonstrate that there is sufficient knowledge and technology available to enable us to reduce vampire bat populations and control this effective vector of the rabies virus.
It is important to consider that the control methods described select only those vampire bats feeding on cattle. Therefore, there are good possibilities that haematophagous bats that continue feeding on wild animals will maintain the species' existence in nature.
Bibliography
Acha, N.P. 1968. Epidemiología de la rabia bovina paralítica transmitida por los quirópteros. Boletín de la Oficina Sanitaria Panamericana, 64: 411-430.
Amaya, R.M. & Carrera, T.B. 1976. Determinación de residuos de warfarina en bovinos tratados con vampirinit III. Técnica Pecuaria en México, 33: 74.
Anderson, S. & Knox, V.V. 1967. Recent mammals of the world. A synopsis of families. New York, NY, USA, Ronald Press Company.
Arellano, C. 1980. Avances sobre la epizootiología de la rabia paralítica bovina en México. Sesiones Públicas de la Academia Veterinaria Mexicana A.C. 177(40).
Atanasiu, P., Fuenzalida, E., Acha, N.P. & Szyfres, B. 1968. Inmunidad antirrábica en bovinos vacunados. Boletín de la Oficina Sanitaria Panamericana, 64: 431-440.
Batalla, D., Sureau, P., Arellano, C. & Morales, J. 1971. Resúmenes de la XII Reunión Anual del Instituto Nacional de Investigaciones Pecuarias. México.
Bullard, R.W., Thompson, R.D. & Holguin, G. 1976. Diphenadione residues in tissues of cattle. J. Agric. Food Chem., 24: 261-263.
Cabrera, A. 1957. Catálogo de los mamíferos de América del Sur. Revista del Museo Argentino de Ciencias Naturales, Bernardino Rivadavia, Argentina. Ciencias Zoológicas, 1: 307.
Campos-Vela, J. 1972. Identificación de la ingesta gástrica pare determinar los huéspedes del murciélago Desmodus rotundus como contribución a la epizootiología de la rabia en México. DVM diss. Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad de México.
Carini, A. 1913. Defendiendo un diagnóstico. Argentina Biología, 161.
De Anda, L.D., Velarde, F.I. & Flores-Crespo, R. 1971. Evaluación de tres vampiricidas comerciales de aplicación tópica en el control de vampiros Desmodus rotundus. Técnica Pecuaria en México, 28: 31.
FAO/OIE/WHO. 1969. Animal Health Yearbook 1968, p. 117, 151. Rome, FAO.
FAO/OIE/WHO. 1979. Animal Health Yearbook 1978, p. 38, 54. Rome, FAO.
FAO/OIE/WHO. 1986. Animal Health Yearbook 1985, p. 44, 54, 64. Rome, FAO.
Flores-Crespo, R. 1978. La rabia, los murciélagos y el control de los hematófagos. In R. Moreno-Chan, ed. Ciencia Veterinaria, Vol. 2. Ciudad de México, Universidad Nacional Autónoma de México.
Flores-Crespo, R. & Arellano-Sota, C. 1988. Biology and control of the vampire bat. In G.M. Baer, ed. The natural history of rabies. New York, NY, USA, Academic Press.
Flores-Crespo, R. & Said, F.S. 1972. Reducción de la dosis de anticoagulantes (difenadione) pare el control de los vampiros. Técnica Pecuaria en México, 23: 19.
Flores-Crespo, R., Burns, R.J. & Said, F.S. 1974. Evaluación de una técnica pare combatir los vampiros en sus refugios. Boletín de la Oficina Sanitaria Panamericana, 76: 427.
Flores-Crespo, R., Ibarra, F. & De Anda, L.D. 1976. Vampirinys II, un producto utilizable en tres métodos pare el control del murciélago hematófago. Técnica Pecuaria en México, 30: 67.
Flores-Crespo, R., Linhart, S.B. & Burns, R.J. 1971. Comportamiento del vampiro Desmodus rotundus durante su alimentación en ganado bovino en cautiverio. Técnica Pecuaria en México 18: 40.
Flores-Crespo, R., Linhart, S.B. & Burns, R.J. 1972. Comportamiento del vampiro Desmodus rotundus en cautiverio. Southwest. Nat., 17: 139.
Flores-Crespo, R., Said Fernández, S., Burns, R.J. & Mitchell, G.C. 1974. Observaciones sobre el comportamiento del vampiro común (Desmodus rotundus) al alimentarse en condiciones naturales. Técnica Pecuaria en México, 27: 39.
Flores-Crespo, R., Linhart, S.B., Burns, R.J. & Mitchell, G.C. 1976. Foraging behaviour of the common vampire bat related to moonlight. J. Mammal., 53: 366-368.
Flores-Crespo, R., Said Fernández, S., De Anda López, D., Ibarra Velarde, F. & Anaya, R.M. 1979. Nueva técnica pare el combate de los vampiros: warfarina por vía intramuscular al ganado bovino. Boletín de la Oficina Sanitaria Panamericana, 87: 283-299.
Grasso, R. 1955. Libros de la Academia de Medicina de México, p. 1758.
Gut, H.J. 1959. A pleistocene vampire bat from Florida. J. Mammal., 40: 534.
Hernández, B.E. 1976. Resúmenes de la XIII Reunión Anual del Instituto Nacional de Investigaciones Pecuarias. México.
Koopan, K.F. 1958. A fossil vampire bat from Cuba. Breviera, 90: 1.
Lopez-Forment, W., Schmidt, U. & Greenhall, A.M. 1971. Movement and population studies of the vampire bat (Desmodus rotundus) in Mexico. J. Mammal., 52: 227.
Málaga, A.A. 1959. La rabia de los murciélagos como problema veterinario y de salud pública. Ciencia Veterinaria, 4: 520. Ciudad de México, Universidad Nacional Autónoma de México.
Mitchell, G.C., Burns, R.J. & Kolz, A.L. 1973. Rastreo del comportamiento nocturno de los murciélagos vampiros por radiotelemetría. Técnica Pecuaria en México, 24: 47.
Park, H. & Hall, E.R. 1951. In Trans. Kansas Acad. Sci. 1951, p. 54-64.
Pawan, J.L. 1936. In Ann. Trop. Med. Parasitol., 30: 137-156.
Said, F.S. 1973. Determinación de la dosis fetal pare el vampiro común Desmodus rotundus de tres compuestos químicos. Técnica Pecuaria en México, 25: 38.
Telles Girón, A. 1945. Identificación del vampiro agente transmisor del derriengue y sugestiones para su captura y exterminio. Secretaría de Agricultura y Fomento, Dirección General de Ganadería. Publication No. 2.
Thompson, R.D., Mitchell, G.C. & Burns, R.J. 1971. Vampire bat control by systemic treatment of livestock with an anticoagulant. Science, 177: 806-808.
Villa-Ramírez, B. 1966. Los murciélagos de México. Ciudad de México, Instituto de Biología, Universidad Nacional Autónoma de México.
Villa-Ramírez, B. 1976. Biología de los murciélagos hematófagos. In R. Moreno-Chan. ed. Ciencia Veterinaria, Vol. 1. Ciudad de México, Universidad Nacional Autónoma de México.
Wimsatt, W.A. 1969. Transient behaviour, nocturnal activity patterns, and feeding efficiency of vampire bats (Desmodus rotundus) under natural conditions. J. Mammal., 50: 233-244.
