Observations of the common vampire bat (Desmodus rotundus) and the hairy-legged vampire bat (Diphylla ecaudata) in captivity

Mammalian Biology

Mamm. biol. 67 (2002) 65±78 ã Urban & Fischer Verlag http://www.urbanfischer.de/journals/mammbiol

Zeitschrift fuÈr SaÈugetierkunde

Original investigation

Observations of the common vampire bat (Desmodus rotundus) and the hairy-legged vampire bat (Diphylla ecaudata) in captivity Von H. A. DELPIETRO and R. G. RUSSO Servicio Nacional de Sanidad y Calidad Agroalimentaria, Posadas, Argentina Receipt of Ms. 03. 01. 2001 Acceptance of Ms. 08. 10. 2001

Abstract We investigated roosting patterns, reproduction, morphometry, and ontogeny of a group of common vampire bats (Desmodus rotundus) and a group of the hairy-legged vampire bats (Diphylla ecaudata) both maintained for > 3 years in captivity. The basic social structure observed in Desmodus was of a ªprincipal colonyº or ªharemº composed of females and their offspring and a few adult males, termed ªresident malesº and a separate group of the other males, termed ªnon-resident malesº. The roosting patterns of Diphylla differed little from those observed in Desmodus, but the hierarchical segregation of non-resident males appeared to be less strict. In both species the non-resident males are accepted into the principal colony when the ambient temperature lowers. This behavior suggests social thermoregulation. Parturition of both species occurred once a year, and most of the births took place in spring or summer. The average duration of palpable pregnancy and lactation was longer in Desmodus than in Diphylla. In both species some lactating females that had lost their young continued suckling the babies of other females. Desmodus is larger in size than Diphylla. This may be related to the size and type of prey; Desmodus preys principally on large mammals and Diphylla preys on birds. We observed female biased sexual dimorphism in Desmodus and isometrical sexes in Diphylla. This may be related to the differential duration of lactation and maternal care periods, as the breeding cycle in Desmodus is longer than in Diphylla. The average time of reaching maturity: epiphysis closure of wing bones, adult weight, scrotal testes, and first pregnancy, as well as the first flight time and the time when males begin to roost apart from the principal colony, were later in Desmodus than in Diphylla. The variation between the two genera for duration of ontogeny and maternal care periods may be related to the learning needs for predation on different types of prey. Key words: Desmodus, Diphylla, roosting patterns, morphometry, reproduction

Introduction The common vampire bat Desmodus rotundus is an haematophagus bat that feeds principally on mammals. At present Des1616-5047/02/67/02-065 $ 15.00/0.

modus is rather rare in undisturbed tropical ecosystems, but is abundant and lives as eusynanthropic species in most of the tropi-

66

H. A. DELPIETRO and R. G. RUSSO

cal and temperate cattle-raising ecosystems of Mexico, Central and South America (Crespo et al. 1961; Constantine 1979; Greenhall et al. 1983; Delpietro et al. 1992; Delpietro and Russo 1996). Observations in captivity (Schmidt et al. 1978; Lord et al. 1981; Park 1991) and in nature (Wilkinson 1985 a, b) indicate that Desmodus has a highly developed social structure. The studies on morphometry of adult Desmodus indicate a marked dimorphism in size (Crespo et al. 1961; Goodwin and Greenhall 1961; Wimsatt 1969), but information on the morphometry of newborn is scarce (Crespo et al. 1961; Burns 1970). An aseasonal poliestry with births distributed through out the year was observed in Desmodus in different parts of America (De Verteuil and Urich 1936; Wimsatt and Trapido 1952; Goodwin and Greenhall 1961; Lhanggut and Achaval 1972; Greenhall et al. 1993). Nevertheless, observations from Argentina and southern Brazil indicate the existence of a spring peak of births (Crespo et al. 1961; Lord 1992). Gestation-period estimates vary between 3 to 7 1/2 months. (De Verteuil and Urich 1936; Wimsatt and Trapido 1952; Schmidt 1974; Greenhall et al. 1983; Greenhall et al. 1993). The hairy-legged vampire bat Diphylla ecaudata is a scarce haematophagus bat that feeds on birds (Dalquest 1955; Hoyt and Altembach 1981; Greenhall et al. 1984). Studies on the morphometry of Diphylla are scarce (Ruschi 1951; Redell 1968; Bhatnagar 1978). Some authors indicate aseasonal polyestry (Bhatnagar 1978; Wilson 1979; Hoyt and Altembach 1981), although Dalquest (1955) observed a well-defined breeding season in Mexico. We found no references on gestation or ontogeny. The maintenance of groups of vampire bats in captivity which are permitted to segregate naturally, allows the observation of aspects that are difficult to study in nature such as: roosting patterns, duration of gestation and lactation, repeated measurements of growth and weight of newborn, etc. Various reports indicate that Desmodus can

live in captivity for years (De Verteuil and Urich 1936; Trapido 1946; Wimsatt 1962; Wimsatt and Guerriere 1962; Burns 1970, 1972; Schmidt and Manske 1973; Lord et al. 1981), but the maintenance of Diphylla is reported as difficult (Bhatnagar 1978; Hoyt and Altembach 1981). The purpose of this study was to observe roosting patterns, reproduction, newborn morphometry and ontogeny of the common vampire bat Desmodus rotundus and of the hairy-legged vampire bat Diphylla ecaudata, maintained as social groups in captivity.

Material and methods Captivity conditions: Observations were made in the Laboratorio Regional Posadas belonging to the Servicio Nacional de Sanidad y Calidad Agroalimentaria, located in a rural area 10 km SW of the City of Posadas (27°22' S, 55°5' W; 133 m above sea level), Province of Misiones, Argentina. The climate is humid subtropical with no dry season, the annual mean temperature is 21 °C, and the mean rainfall 1 623 mm (Camarata 1982). The bats were kept in a rectangular cage made of wood and wire mesh 3.8 m wide ´ 3.2 m deep and 2.2 m high, inside a building. The building had a door and window of wire mesh. Thus, the illumination and ventilation of the cage did not differ from what is observed in nature of Desmodus roosts inside buildings. For the purpose of providing physical exercise for the caged bats, the cage was divided longitudinally by a wire mesh wall with an opening 2 ´ 0.6 on one end that allowed communication between the two sides. Thus, the bats had to make a ªU-formº flight (ca. 7.6 m) to move from one to the other corner of the closed end of the cage. The division also facilitated bat capture and diminished the risk of harming them. In the upper corners and other places of the cage roof wire mesh patches were placed for bat roosting. The cage floor was covered with a layer of wood sawdust. To recreate natural conditions, when the cage floor was cleaned we did not take out all the fecal matter deposited below the bat roosts. The study was made under natural climatic conditions. However, on the coldest winter days we did not allow the cage temperature to fall below 9 °C, because this is the minimum temperature that we observed inside Desmodus roosts in Argentina. Animals: The group of Desmodus formed initially of adults (5 males and 7 females) was observed

Observations on Desmodus rotundus and Diphylla ecaudata from 9 March, 1992 to 30 April, 1996. These bats were captured from an abandoned warehouse located < 5 km SW of the laboratory from the phytogeographical region termed ªSubtropical Forests of the east and south of Brazilº (Hueck 1966). The bats were marked by placing numbered bands on their forearms (left male, right female). The group of Diphylla formed initially of adults (8 males and 5 females), was observed from 12 November, 1996 to l6 December, 2000. The bats were from the phytogeographical region termed ªSubtropical Forests of the east and south of Brazilº (Hueck, 1966). They were captured on 8 November, 1996 in a natural stone cave located in a rural area near the town of Major Gercino, Santa Catarina state, Brazil, 27°24' S, 48°55' W. These bats were marked by placing numbered bands on their forearms (left male, right female). They were transported to the laboratory by car and fed on live hens during the trip. The capture and removal of these bats from Brazil were authorized by the Health and Customs authorities of Brazil and Argentina. Weight and measurement methods: Measurements of lengths were taken with Vernier and body mass with an electronic scale (0.01 g precision). We considered the ªocular diameterº to be the diameter between the inner and outer canthus of the eye. To measure the ocular diameter the bats were anesthetized with ethylic ether. The newborns were weighed and measured for the first time at 8±12 h after birth by removing them carefully from the nipple, and after weighing and measuring, replacing them to the mother and returning them both to the cage. Thereafter, young and adults were always weighed between 10.00 and 12.00 h, because in haematophagus bats, body mass varies greatly during the circadian cycle due to the great volume of the blood meal. For the same reason, and due to the large size of the fetus, we only registered the weights of females which were not palpably pregnant. Feeding: The diet of Desmodus consisted of defibrinated (stirring with a twig) bovine blood administered in dishes at ambient temperature ad libitum. The diet of Diphylla consisted of live hens at a ratio of 1 for each bat, that were placed every night. The hens retired the following morning. Thus, most of the hens survived and could be reused every 14 days. Group observation: The group was observed from inside the cage for ca. 10 min twice a day; in the morning during the cleaning task (10.00±12.00 h) and in the afternoon when feeding (ca. 19.00 h). Observations of the group were also made from outside the cage (6 m away) for about 10 min every 20 (+/±1) nights. This observation was made between 21.00 and 23.00 h using binoculars and il-

67

luminating the cage with a red 40 W electrical lamp. Principal observations of the group were: 1) weighing and measuring the newborn, 2) observations of roosting patterns, 3) registration of the first flight of the young; we registered as ªfirst flightº the first observation of a complete ªU formº flight from one corner to the other of the close end of the cage, 4) registration of the moment when young males began roosting apart from the principal colony, 5) estimation of the approximate duration (in days) of the regurgitation feeding period. Individual observation: Each week (+/±1 day) all bats were captured between 08.00 and 10.00 h. The main objectives were: 1) diagnoses of pregnancy by palpation; achieved by an assistant pinning the wings behind the back and holding the extended legs while the investigator softly massaged the abdomen to feel the uterus, 2) registration of the duration of lactation determined by extruding milk through squeezing the mammary glands and nipples, 3) study of ontogeny of young by weighing, measuring the forearm and observing epiphyseal-diaphyseal fusion of the metacarpal and phalangeal bones by transilluminating the wing with a 100 W electric lamp. Direct observation of the embryos (complementary fieldwork): The main objectives were: 1) determination of the minimum size and characteristics of embryos perceived by external palpation, 2) estimation of the approximate age of these embryos. In July, 1992, 7 of 47 pregnant Desmodus females captured in the wild were selected as those with the smallest embryos perceived by palpation. They were taken to the laboratory, sacrificed with an overdose of ether and their uteruses extracted to measure the diameter of the gravid horn. Embryos were then removed for measurement.

Results Group observation: Throughout the study the group of Desmodus remained in good health, exhibiting a clean and brilliant coat and maintaining their weights similar to those at the moment of capture (Tab. 1). From the beginning of captivity the bats chose one corner on the closed end of the cage (the darkest) for roosting and remained in close contact, in a single group for the first 24 hours. Afterwards the bats segregated themselves as follows: 1) the largest group (principal colony) comprising all

68

Desmodus rotundus

Diphylla ecudata

Adult

Newborn

Weight* Male Observations

Female Male

Ocular Weight* Forearm* Weight* Forearm* Ocular Weight* Forearm* diamediameFemale ter** Male Female Male Female Male Female Male Female ter** Male Female Male Female

8

5

8

Average

42.9

50.6

62.9

Median

42.7

49.4

Minimum

39.5

Maximum

SD t test

Newborn

Forearm*

5

Sum

Adult

7

6

9

67.9

2.9

8.5

9.6

62.8

67.3

2.9

8.4

46

61.7

65

2.8

8

46.3

56.7

64.5

71

3

9.5

214.7

404.6

314.9

20.2

51.2

4

1

2.46 t = 3.85, P < 0.003

54.3 1.84

t = 5.36, P 5 0.001

0.09

0.54 t = 2.7, P < 0.02

10 8.2 11 86.7 0.88

6

8

7

5

8

5

6

5

6

29.1

30.9

26

26.4

51.8

52.7

4

7.5

29.2

31.5

26.6

26.4

51.8

52

4

28

28.3

23.8

25.2

50.4

51

30

32.5

27.5

28.1

52.7

55.3

414.1

263.7

175

247

0.7 t = 2.63, P < 0.03

1.6

182.4

132

1.5 t = 0.41, P = 0.69

1.21

0.77 t = 1.46, P = 0.17

1.67

5

6

7.5

26.2

26.4

7.5

7.6

26.3

26.1

3.8

6.9

6.7

25.9

25.2

4.1

8.3

8.2

26.4

28.3

37.7

45.2

24 0.11

0.52 t = 0.02, P = 0.98

0.54

131 0.2 t = 0.38 P = 0.71

158.4 1.17

H. A. DELPIETRO and R. G. RUSSO

Table 1. Morphometry, summary of statistics, weight values in g, length values in mm and t tests performed to compare the differences between males and females (*) Values corresponding to bats of the original group, 30 days after being placed captivity ± (**) Values corresponding to the left eye of adult females

Observations on Desmodus rotundus and Diphylla ecaudata the females and some adult males (resident males) occupying the same corner on the closed end of the cage, 2) the rest of the males (non-resident males) and occasionally a female formed a small group (secondary group) which roosted in the opposed corner (on the open end of the cage), or hung solitarily separated from both groups. The ratio of resident to non-resident males was generally < 1. Agonistic behavior was not observed among the resident males, but they chased out the non-resident males if they approached the principal colony. Changes between groups among adult males were observed with males of the principal colony roosting alone or with the secondary group and vice-versa. Most of these changes remained although some reverted later. Most of the females remained constantly with the principal colony. This roosting pattern remained consistent throughout the study except when the temperature fell below 11 °C, when all or most of the bats roosted together in the principal colony. The Desmodus were always fearful of human presence. They flew quickly whenever anyone came within less than 3 m of their roost. When captured, they defended themselves fiercely, hitting with their wings, emitting strong vocalizations ana biting anything within reach. The group of Diphylla likewise remained in good health throughout the study, exhibiting a clean and brilliant coat, and maintaining their weights similar to those at the moment of capture (Tab. 1). From the beginning of captivity the bats chose the same corner of the cage for roosting that Desmodus had chosen previously and they stayed in close contact as a single group for the first 2 days. After the 3rd day some males roosted apart from the principal colony. The roosting patterns of Diphylla resembled those of Desmodus. The main differences were: the ratio resident to non-resident male was generally > 1, the presence of females roosting temporarily with non-resident males was more frequent and all (or most) of the non-resident males were roosting with the principal colony when the temperature fell below 14 °C (Fig. 1). Diphylla was observed to be

69

Fig. 1. (Diphylla ecaudata) principal colony photographed on 4 July 2000 in the morning, when the temperature inside the cage was 14 °C. The principal colony was composed of 14 bats: 5 adult males, 5 adult females and 4 subadults (3 females and 1 male). At this moment the total number of bats in the cage was 15, only a single adult male was roosting apart from the principal colony.

more docile than Desmodus. The bats did not fly even when persons approached closer than 1 m to the group, and often it was possible to touch the back of a bat without them or their partners taking flight. When Diphylla were captured, they defended themselves by attempting to escape from the hand, but they generally did not bite or emit strong vocalizations. Morphometry: Desmodus was larger than Diphylla (Tab. 1), the average differences between adults were significant (tbiomass = 14.09, P 5 0.0001; tforearm = 15.48, P 5 0.0001). The average biomass ratio Desmodus/Diphylla was 1.79. Conversely, the eye size of Desmodus was smaller than of Diphylla, the average differences between adult ocular diameter (Tab. 1) were significant (t = 20.2, P 5 0.0001). Desmodus newborns were larger than Diphylla newborns (Tab. 1), but relatively smaller compared with the adult size; the newborn/adult biomass ratio was 0.19 in Desmodus and 0.29 in Diphylla. The difference was significant (v2 = 5.24, P < 0.03). In Desmodus female biased sexual dimorphism in size was seen. In Diphylla dimorphism was not evident (Tab. 1).

70

H. A. DELPIETRO and R. G. RUSSO

Reproduction: In both Desmodus and Diphylla the birth of the second generation was observed (offspring of captive-born bats). The females of both species gave birth once a year and most of the births took place in spring or Summer; Desmodus 94% (n = 17; v2 = 9.07, P < 0.003); Diphylla 92% (n = 13; v2 = 4.51, P < 0.04). The births of Desmodus mainly occurred in November±December (65%) but in Diphylla during September±October (50%). The average age at first pregnancy and also the duration of palpable pregnancy were longer in Desmodus than in Diphylla (Tab. 2); the differences were significant (t = 5.52, P < 0.002) and (t = 4.08, P < 0.003), respectively. In both species the body of newborn was covered with hair and the eyes were open. During the first postnatal days the baby remained tightly attached to its mother's nipple; Desmodus (X = 18, n = 3); Diphylla (X = 17, n = 4). Noteworthy of the newborn Diphylla is the large size of the eyes and that they maintain constantly open, attentive to objects that move in their environment (Fig. 2). The average lactating period was longer in Desmodus than in Diphylla (Tab. 2), with the differences being significantly different (t = 6.35, P 5 0.001). In both species we noted that lactating females that had lost their young continued suckling the babies of other females (2 from 7 Desmodus and 1 from 4 Diphylla). In those cases the foster and the biological mothers usually weaned the offspring and became pregnant again at the same time. The young of the two species were fed by their mothers by regurgitation. The regurgitation feeding was longer in Desmodus than in Diphylla (Tab. 2), although the difference was not significant. Ontogeny: The average ages for attaining epiphyseal fusion and adult weight (Tab. 2), were older for Desmodus than for Diphylla (t = 2.79, P < 0.02; t = 10.35, P 5 0.001), respectively. The observation of the first flight was later in Desmodus than in Diphylla (t = 5.30, P < 0.002). The age at which young males began roosting

apart from the principal colony was older for Desmodus than for Diphylla (t = 5.75, P < 0.002). Age of first pregnancy was older for Desmodus than for Diphylla (t = 5.52, P < 0.002). Age for scrotal testes was older for Desmodus than for Diphylla but the difference was not significant (Tab. 2). Direct observation and embryo age estimation: In those Desmodus females that had the smallest externally perceived embryos, the diameter of the gravid uterus ranged from 6.7 to 7.8 mm (Fig. 3). Upon removing the uterus and chorion, the embryos, including the vitelline and chorionic sacs, measured between 4 to 5 mm (Fig. 3). The embryos themselves were disk shaped (without macroscopic morphological differentiation) and ranged between 1 to 1.6 mm (Fig. 3). The presence of vitelline and chorionic sacs suggested that the bat embryos were not less than 15 days of gestation, because in other species with long gestation periods, such as in man and horses, these structures appear at the end of the second week of gestation (Michel and Schwarze 1970; Hib 1999).

Discussion Our observations on the ease of maintaining Desmodus in captivity are consistent with those reported previously (de Verteuil and Urich 1936; Trapido 1946; Wimsatt 1962, 1969; Wimsatt and Guerriere 1962; Burns 1972; Schmidt et al. 1980; Lord et al. 1981). To our knowledge, the maintenance and breeding of Diphylla in captivity has not been previously reported. This may be related to the small size of the cages previously used, which did not permit extensive flying (Bhatnagar 1978; Hoyt and Altembach 1981). The fact that the original groups of Desmodus and Diphylla were captured within the same phytogeographical region and at nearly the same latitude, and were maintained under similar conditions in captivity, facilitated the comparison of observations. Roosting patterns: Our observations of Desmodus are consistent with those reports

Table 2. Reproductive and ontogeny data (in days) of haematophagus bats observed in captivity (*) First observation of a young male roosting apart from the main goup ± (**) Last obsrvation of a regurgitation-feeding bout Desmodus rotundus

Observations

Bone Adult Roost- Scrotal First Regurgita- PalLacFirst fusion weight ing tests preg- tion feed- pable tating flight appart nancy ing (**) preg(*) nancy

Bone Adult Roost- Scrotal First Regurgitafusion weight ing tests preg- tion feedappart nancy ing (**) (*)

17

7

4

7

5

4

3

4

2

9

6

4

7

6

4

2

4

3

Average

150

278

79

255

356

377

339

515

348

141

217

57

215

178

235

231

367

223

Median

150

278

77

240

353

380

343

514

348

142

218

56

210

187

231

231

361

221

Minimum

146

243

73

220

327

329

320

453

335

131

193

54

191

121

209

217

355

205

Maximum

155

304

89

310

397

421

355

578

361

150

238

63

248

203

269

245

391

243

2 547

1 950

317

1 789

1 780

1 511

1 018

2 060

696

1 272

1 302

230

1 508

1 068

940

462

1 468

669

3

19

7

32

26

41

17

51

18

6

16

4

20

30

27

20

16

19

Sum SD

Observations on Desmodus rotundus and Diphylla ecaudata

PalLacFirst pable tating flight pregnancy

Diphylla ecaudata

71

72

H. A. DELPIETRO and R. G. RUSSO

Fig. 2. (Diphylla ecaudata) newborn of between 8 and 12 h of life. When the young are removed from the nipple, eyes remain open constantly and attentive to environmental movements, while soft vocalizations are responded by their mother.

Fig. 3. (Desmodus rotundus) Above: the diameter of the smaller gravid uterus that was perceivable by external palpation ranged between 6.7 and 7.8 mm. Below: After removal of the uterus and chorion, the measurement of the embryos (with vitelline and chorionic sacs included) ranged from 4 to 5 mm. Below (indicated by arrow): the embryos themselves had a disk shape with diameters ranging from 1 to 1.6 mm.

regarding the existence of a principal colony or harem and subordinate males roosting separately (Wilkinson 1985 a, b; Park 1991), but they differ in relation to the harem composition. We usually observed 2 or more resident males cohabiting in harmony within the principal colony. These males sometimes remained very close to one another and we did not observe agonistic behavior between them. The coexistence of several resident males within the principal colony was frequently observed in Desmodus in nature, mainly in roosts of more than 30 bats (Delpietro and Russo unpublished data), and this was also observed in the Jamaican fruit-eating bat (Artibeus jamaicensis) (Ortega and Arita 1999). This behavior could be related with the presence of a surplus of females for a single male and/ or the possibility that several resident males could form an alliance to defend the female group against other males. The observation that social exclusion of non-resident males diminishes when the environmental temperature fall is not surprising when considering that: 1) Desmodus do not hibernate (Greenhall et al. 1983), 2) thus requiring energy to maintain corporal temperature (McNab 1969, 1973), and 3) has a very limited thermoregulation capacity (Wimsatt 1962). On the other hand, social thermoregulation occurs in other Phyllostomidae (Howell 1976; Lewis 1992). In South America this behavior can favor bats that live in temperate regions with rigorous winters, as in Uruguay, the central part of Argentina and Chile and southeastern Brazil (Mann 1954; Crespo et al. 1961; Langguth and Achaval 1972; Lord 1992) and those bats that live in mountainous areas at high elevations above sea level (Crespo 1941; Tramsitt and Valdivieso 1962). The roosting patterns of Diphylla differs little from that observed in Desmodus, but the hierarchical social segregation of non-resident males seems to be less strict. Defensive behavior: The quick retreat from the presence of humans and the ferocious bites and strident vocalizations that characterize the defensive behavior of most of Desmodus when captured, contrast with

Observations on Desmodus rotundus and Diphylla ecaudata the meek behavior and the passivity observed in Diphylla under the same circumstances. This coincides with observations in nature within the roosts of both species (Bredt et al. 1999; Delpietro and Russo unpublished data; Lord personal communication), and suggests the existence of different defensive behaviors against predators. A rapid escape seems important for Desmodus because it cannot hide under the short fur of its prey and is thus exposed to the attack of predators (Delpietro et al. 1992). After feeding Desmodus invariably seeks flight (Greenhall et al. 1969). On the other hand, mild movements are favorable for Diphylla because, while feeding they remain hidden within the plumage of its prey (Hoyt and Altembach 1981). The plumage of the prey appears to be a secure hiding place for Diphylla, because after feeding, it frequently remains up to 50 min on the prey, motionless and urinating copiously to eliminate the excess water of its ingesta (Delpietro and Russo unpublished data). Reproduction: The palpable pregnancy period of Desmodus and the estimated age of embryos observed in necropsy suggest that the gestation period of this species could last between 165 and 180 days. In comparison with estimates of others that studied Desmodus in captivity our estimate is longer than those of De Verteuil and Urich (1936) and Wimsatt and Trapido (1952) and slightly shorter than Schmidt (1974). The gestation period of Diphylla could be approximately 14 days shorter than Desmodus, as its palpable pregnancy period is 14 days shorter. Observations that in both species most of the births happened in spring and summer agrees with previous observations for Desmodus in Argentina and southern Brazil (Crespo et al. 1961; Lord 1992) and in Diphylla in Mexico (Dalquest 1955) concerning the existence of a well-defined breeding season. The spring-summer births of Desmodus and Diphylla coincide with the birth of most of domestic and wild mammal and avian preys in Argentina, Chile, Paraguay, Uruguay, and the south of Brazil (Mann 1954; Cabrera and Yepes

73

1960; Olrog 1965; Ostrowsky 1977; de la PenÄa 1995; Hayssen et al. 1993). The young naive prey facilitates the forage of the young bats (Arellano et al. 1971), keeping in mind that the beginning of predation is the most critical period in the life of vampire bats (Schmidt and Manske 1973; Schmidt et al. 1980; Wilkinson 1985 a, b). Another advantage of a defined breeding season is the joint care oft heir young by the females, including the possibility that young can obtain milk from other lactating females if their own mothers fail to return to the roost for a night (Schmidt et al. 1980). A defined breeding season also facilitates that females, which have lost their own young, continue suckling the babies of other females, as was observed for both species in this study. The suckling of babies by mothers other than their own has been observed previously in Desmodus (Schmidt et al. 1980). Our observation of this behavior appears to be the first for Diphylla. This behavior may be related to kin selection because it was only observed in some Desmodus and Diphylla females. Nevertheless, we cannot ascertain this because in the cases observed in both species the foster and the biological mothers belonged to the original group. However, we cannot discard mutual benefit, because this behavior can also favor synchronization. In both species the foster and the biological mothers usually finished lactation and were pregnant again synchronously. Ontogeny and maternal care period: The growth from birth to adulthood in Desmodus was slower than that for Diphylla. The average age at weaning for Desmodus was 278 days, before they reach adult weight. After weaning, mothers feed their young by regurgitation blood for up to an average of 348 days. Young Diphylla reach adult weight before weaning at an average time of 178 days. They then continue suckling and being fed regurgitated blood until than average of 223 days of age. Functional development was also slower in Desmodus than in Diphylla. The observed long duration of ontogenesis and maternal care in Desmodus agrees with previous reports

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H. A. DELPIETRO and R. G. RUSSO

(Schmidt and Manske 1973; Schmidt et al. 1980). The differences in the length of ontogeny and maternal care between Desmodus and Diphylla may be related to their respective prey types and the learning required for each species. Desmodus needs a long learning period due to their variety in morphology, size, habits, and modes of defense of the mammal preys (Greenhall et al. 1969, 1983, 1993; Delpietro 1989). On the other hand, feeding on mammals provides increased risk of predation because Desmodus is readily visible on the surface of the short fur of the mammal, or on the bare ground while feeding on the foot of the prey (Delpietro et al. 1994). The observation that Desmodus, in nature, does not demonstrate a qualitative preference for the blood of certain species, but rather prefers those species that are more abundant, indicates the importance for training of young by the adults (Delpietro et al. 1992). Diphylla feeds on diurnal birds which it attacks in the roosts when they sleep (Greenhall et al. 1984). The small possibilities that birds have to defend themselves while sleeping at night, the thick plumage offering the bats a hiding place from predators during the process of feeding, and the smaller degree of encephalization of Diphylla compared to Desmodus (Mann 1960; Pirlot and Stephan 1970; Stephan 1977), all suggest that feeding on birds required less learning. Morphometry: The size differences between Desmodus and Diphylla can be related to the type of prey, because haematophagus bats, preparing to fed, remove with a single bite a piece of skin exposing the subcutaneous tissue from which they lap the blood (Greenhall 1972; Greenhall et al. 1983). Without doubt larger size and force is necessary to perforate the thick skin of large or medium sized mammals than to perforate the thinner skin of birds. The large size of the eyes of Diphylla suggests that visual detection of prey may play a greater role than in Desmodus. Birds, due to their smaller size and insulating plumage, may be more difficult targets for heat and/ or breathing and noises detection, which

are the main senses used by Desmodus to find mammals (KuÈrten and Schmidt 1984; Schmidt et al. 1991). The female biased sexual dimorphism in size observed in Desmodus agrees with previous reports (Crespo et al. 1961; Goodwin and Greenhall 1961; Wimsatt 1969). Our results indicate that this dimorphism is observed from birth. In Diphylla sexual dimorphism was not observed. In insectivorous bat species, female biased sexual dimorphism is attributed to the large fetuses demand (Myers 1978); however, this would not explain the differences between Desmodus and Diphylla, because the fetus of Desmodus is relatively smaller than that of Diphylla where the sexes are isometrical. The ªBig Motherº hypothesis (Ralls 1976) appears to be more appropriate to explain these differences. Desmodus females have one offspring per year, the pregnancy lasting ca. 6 months, and the average duration of feeding by regurgitation of blood 356 days. This indicates that every year, 2 breeding cycles overlap for 6 months. In other words, while female Desmodus gestate an embryo, care and teaching of predation to the offspring of the previous breeding cycle are also demanded of the mother (Schmidt et al. 1980). To respond to this great energetic demand, female Desmodus must increase food intake without hindering their flight capacity. In nature excessive ingestion adversely affects (and can completely impede) flight (Ditmars and Greenhall 1935; Wimsatt 1969; McFarland and Wimsatt 1969). Thus, the increase in corporal size and the relative smaller fetus of Desmodus may be adaptative responses to reduce the relative load of the blood ingestion. Other possible advantages of a large female are: the reduction of the relative cost of producing milk (Myers 1978) and the reduction in the intersexual competition for food (Ralls 1976), since females of Desmodus are capable of displacing males at the feeding site (Schmidt and van de Flierdt 1973; Lord et al. 1981). The possibility to fly directly to the prey and feeding from a bite made by another bat (Schmidt et al. 1970; Schmidt and Manske 1973) re-

Observations on Desmodus rotundus and Diphylla ecaudata sults in a great saving in the expenditure of energy. Females of Diphylla also have only one offspring per year, but in this species the overlapping of successive breeding cycles is only of few days duration, if any, because the pregnancy lasts approximately 5.5 months and the average duration of feeding the offspring is 223 days. In Diphylla, the less investment of time demanded by the offspring (comparing with Desmodus) could be related to the smallest relative size of females.

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Acknowledgements We thank Dr. Jaime Salvatierra Oporto and Dr. Regis Holtausen Maciel of the Companhia Integrada de Desenvolvimento AgrõÂcola de Santa Catarina, Brazil for their collaboration in Diphylla field collection, and Dr. Rexford Lord, retired from the American Health Organization, for the correction of the English version of the manuscript.

Zusammenfassung Verhaltensbeobachtungen an der GewoÈhnlichen Vampirfledermaus (Desmodus rotundus) und der sich vorwiegend von Vogelblut ernaÈhrenden Vampirfledermaus (Diphylla ecaudata) im Labor Wir beobachteten und dokumentierten die Sozialstruktur, Morphometrie (Entwicklung der KoÈrpergroÈûe), Fortpflanzung und Ontogenese bei einer Gruppe GewoÈhnlicher VampirfledermaÈuse Desmodus rotundus und bei einer Gruppe der sich vorwiegend von Vogelblut ernaÈhrenden Vampirfledermaus Diphylla ecaudata. Beide Gruppen wurden seit mehr als drei Jahren unter aÈhnlichen Bedingungen im Labor gehalten. Die Sozialstruktur bei Desmodus bestand hauptsaÈchlich aus einer Gruppe oder Harem, die aus Weibchen und ihren Jungtieren, einigen adulten ¹ansaÈûigenª MaÈnnchen und abseits haÈngenden, ¹nicht-ansaÈûigenª MaÈnnchen zusammengesetzt war. Die soziale Grundstruktur bei Diphylla war aÈhnlich wie bei Desmodus, doch war die Trennung der nicht-ansaÈûigen MaÈnnchen von der Gruppe weniger deutlich ausgepraÈgt. Die nicht-ansaÈûigen MaÈnnchen von Desmodus wurden bei Umgebungstemperaturen unter 10 °C und von Diphylla bei Umgebungstemperaturen unter 14 °C in die Hauptgruppe aufgenommen. Dieses Verhalten ist wahrscheinlich als soziale Form der Thermoregulation zu interpretieren und koÈnnte vor allem fuÈr Desmodus wichtig sein, der in Gebieten mit mildem Klima aber strengen Wintern wie zum Beispiel in Uruguay, in den Kerngebieten Argentiniens und Chile sowie im Hochgebirge lebt. Bei beiden Arten fanden einmal jaÈhrlich Geburten im FruÈhling bzw. im Sommer statt. Die Schwangerschaft und die SaÈugezeit waren bei Desmodus deutlich laÈnger als bei Diphylla. Einige Weibchen beider Arten, die ihr Junges verloren hatten, saÈugten die Jungen ihrer Artgenossinnen. Desmodus ist groÈûer als Diphylla mit einem VerhaÈltnis der KoÈrpermasse von 1.79. Der GroÈûenunterschied koÈnnte mit der Hauptbeute der beiden Arten zusammenhaÈngen, da sich Desmodus vorwiegend von SaÈugerblut und Diphylla vorwiegend von Vogelblut ernaÈhrt. Die Weibchen von Desmodus sind groÈûer als die MaÈnnchen. Bei Diphylla haben wir hingegen keinen sexuellen Dimorphismus in der GroÈûe gefunden. Dies koÈnnte mit Unterschieden in der SaÈugezeit und der Aufzuchtzeit durch Muttertiere zusammenhaÈngen. Bei Desmodus dauert eine Fortpflanzungsperiode laÈnger als 6 Monate. Die MuÈtter fuÈtterten ihr Junges nach dem EntwoÈhnen, bis die Jungtiere nahezu ein Jahr alt waren. Bei Diphylla hingegen war die Fortpflanzungsperiode wesentlich kuÈrzer. Generell war die Entwicklungszeit der Jungtiere vom Schlieûen der Epiphysenfugen, dem Erreichen des Adultgewichts und der Verlagerung der Hoden in den Hodensack, die erste Schwangerschaft sowie das Erreichen der FlugfaÈhigkeit und die Zeit, in der sich die Jungtiere abseits von der Hauptgruppe haÈngten, dauerte bei Desmodus laÈnger als bei Diphylla. Die Unterschiede bezuÈglich der Dauer der Aufzuchtsperioden und der Entwicklung der Jungtiere bei Desmodus und Diphylla koÈnnten mit dem Grad des Lernens zusammenhaÈngen, der notwendig ist, um die unterschiedlichen Beutetypen (SaÈuger, VoÈgel) zu finden und zu nutzen.

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Authors' addresses: Horacio A. Delpietro, Padre Serrano 1116, 3300 Posadas (e-mail: [email protected]) and Roberto G. Russo, Manzana 233, 3308 Candelaria, Argentina