314 Short Notes

Food sharing behavior in the hairy-legged vampire bat Diphylla ecaudata

CYNTHIA ELIZALDE-ARELLANO1, 5, JUAN CARLOS LÓPEZ-VIDAL1, JOAQUÍN ARROYO-CABRALES2, RODRIGO A. MEDELLÍN3, and JOHN W. LAUNDRÉ4

1Laboratorio de Cordados Terrestres, Depto. Zoología, Escuela Nacional de Ciencias Biológicas, InstitutoPolitécnico Nacional, Carpio y Plan de Ayala s/n, Casco de Santo Tomás, CP. 11340, México D.F.

2Laboratorio de Arqueozoología, Instituto Nacional de Antropología e Historia, Moneda no. 4 Col. Centro,CP. 06060, México D.F.

3Instituto de Ecología, Universidad Nacional Autónoma de México. Ap. Postal 70-275 Circuito exterior,Ciudad Universitaria, CP. 04510 México D.F.

4Instituto de Ecología A.C., Centro Regional Durango, km 5 carr. Durango-Mazatlán, 34100, Durango, Dgo. México

5Corresponding author: E-mail: thiadeno@hotmail.com

Key words: Food sharing, Diphylla ecaudata, hairy-legged vampire bats, feeding behavior, Tamaulipas, Mexico

INTRODUCTION

Diphylla ecaudata is one of three extantvampire bat species. It has a tropical distri-bution, occurring in Mexico from southernTamaulipas through the Gulf of Mexicocoastal states, and continues to CentralAmerica and South America to the centralpart of Brazil. This species inhabits cavesand mines. Relative to Desmodus, Diphyllais considered to be rare and its populationssmall in size – with no more than 50 to 70individuals (Greenhall et al., 1984; Uieda,1996; Elizalde-Arellano, 2003), althoughone population of 500 individuals was re-ported from the state of Puebla, Mexico(Medellín and López-Forment, 1986).

Diphylla ecaudata is the most special-ized vampire bat species, feeding exclusive-ly on bird’s blood while their prey sleepamong the branches of the trees (Villa-R.,1967; Villa-R. et al., 1969; Altenbach,1988; Greenhall, 1988; Uieda, 1992; Uiedaet al., 1992; Schutt and Altenbach, 1997).Because of the scarcity of these bats, thereare few studies about their basic biology(Dalquest, 1955; Villa-R., 1967; Uieda,1996; Elizalde-Arellano, 2003). As a result,their social behavior and the relationshipsamong the individuals of a colony are poor-ly understood.

Because of the sanguivorous food habitsof D. ecaudata, we predict that roost mateswill share blood with conspecifics who failto find prey as does the common vampirebat (Desmodus rotundus) (Wilkinson, 1984,1988b; Altringham, 1996). This altruisticbehavior has been widely studied in D. ro-tundus. It has an important role in their social system because it involves the recog-nition of bats that share blood and paren-tal care when a mother or older sibling feed young (Mills, 1980; Schmidt et al.,1980; Wilkinson, 1984, 1985, 1986, 1987,1988a, 1988b; Schmidt, 1988; Denault andMcFarlane, 1995; Altringham, 1996; Kunzand Hood, 2000). However, there are nopublished observations of this behavior forD. ecaudata. Here we describe observationsthat document for the first time this behav-ior in this species.

MATERIALS AND METHODS

We made our observations in Quintero Cave(22°38’N, 99°02’W) in the Neotropical region of theSierra Madre Oriental, south of Tamaulipas, México(Russell and Raines, 1967). The cave is 522 m long,has a 7-m wide skylight 95 m from the entrance, andhas many lateral chambers with variable water con-tent depending on the dry or wet season. The cave wasan active phosphorite mine (no longer in use), so itsmain tunnel is highly modified to allow access for

Short Notes 315

trucks (Lacaillé, 1995; N. L. Navarro, M. J. TenienteF., and M. L. Franco, unpublished data). There are 14species of bats recorded using this cave (Elizalde-Arellano, 2003) and it is one of the most important batroosts in Mexico (Arita, 1993; Anonymous, 1997;Reddell and Mitchell, 1997).

We captured vampire bats from 18:00 to 08:00 hwith three 10-m mist-nets placed in different sites in-side the cave for four consecutive nights each inNovember 1998, February and July 1999. We record-ed sex, weight and total, forearm, head (from nose tonape), and foot lengths of each vampire captured(DeBlase and Martin, 1981). We assigned each bat toa relative age category based on the visual observa-tion through the transilluminated wings of the pres-ence or absence of cartilaginous joints of the fingerbones (Anthony, 1988). Juveniles had cartilaginouszones clearly visible and lighter than ossified parts ofthe bones. Subadults had cartilaginous zones thatwere thinner than the ones in juveniles but continuevisible and lighter than ossified parts of the bones. Inadults the cartilaginous zones were completely absentand only ossified parts of the bones were observed.While we were in the cave, we maintained bats in a 40× 40 × 55 cm mesh cage for 30 to 40 minutes to re-cord food sharing behavior. We recorded these behav-iors ancillary to the main project of the populationecology and reproduction biology of hairy-leggedvampire bats.

RESULTS

We observed four pairs of hairy-leggedvampire bats while they were inside themesh cage. The bats that shared blood ap-proached each other face to face hangingupside-down, then held each other from theneck with their pollex and licked theirmouths (Fig. 1). Sometimes the recipientheld the donor with one posterior limb bythe pelvis. The bats remained in this posi-tion for about 30 minutes, then they separat-ed and rested next to each other with theirwings around their own body and withclosed eyes. Sometimes they extended theirwings as if they were grooming themselves.

We observed this behavior first in No-vember 1998 between an adult male and a female and between two subadult femalesand it lasted 30 minutes for each pair. OnFebruary 1999, we tested to see if the foodsharing behavior was associated with failedforaging events. We prevented two malevampire bats from feeding by isolating them

FIG. 1. Two hairy-legged vampire bats D. ecaudata hanging up-side-down inside the mesh cage, featuring the altruistic food sharing behavior observed in Quintero cave, Tamaulipas, Mexico. Photo by C. Elizalde-Arellano

for one night inside the mesh cage. The nextmorning we introduced into the cage a preg-nant female captured at 8:40 a.m. that hadeaten the night before. Twenty minutes lat-er, one of the isolated males approached thefemale and she regurgitated some blood.The sharing behavior lasted 32 minutes. On July 1999, this sharing behavior oc-curred again between an adult female and a juvenile male but we did not measure itsduration.

DISCUSSION

Although we present only four observa-tions, the behavior described above in D. ecaudata has never been documented be-fore. This behavior seems to coincide withthe altruistic behavior shown by D. rotun-dus (Wilkinson, 1984; Schmidt, 1988). Thebehavior in D. rotundus is elicited when a bat fails to find a prey and returns to the colony roost where it obtains a meal as regurgitated blood from a roost mate(Wilkinson, 1984, 1988b; Altringham,1996). This behavior is important in the social system of the common vampire batbecause it involves the recognition and reciprocity of the individuals that shareblood and is a form of parental care betweenfemales and their young (Mills, 1980;Schmidt et al., 1980; Wilkinson, 1984,1985, 1986, 1987, 1988a, 1988b; Schmidt,1988; Altringham, 1996).

The experiment with the adult males andfemale of D. ecaudata suggests that thissharing behavior may be associated withobtaining food after an unsuccessful forag-ing period similar to D. rotundus (Mills,1980; Wilkinson, 1984, 1988a; Kunz andHood, 2000). Although D. rotundus feedson a variety of domestic or wild mammals,birds, and sometimes reptiles (Greenhall etal., 1983; Greenhall, 1988), they frequent-ly fail to find prey to feed on. This failure isrelated to the age of the bats with a 30%

failure rate if they are less than two yearsold, and 8% if they are older (Wilkinson,1984, 1988a). Food sharing then can be im-portant in enhancing the probability of sur-vive of young D. rotundus, who would dieof starvation after 60 h without a meal (Du-gatkin, 1997).

Because D. ecaudata feeds exclusivelyon bird’s blood, we predict that failed at-tempts to find a prey would be more fre-quent than experienced by D. rotundus,which feeds on many other kinds of prey.Juveniles would also most likely be lesssuccessful than adults and would probablyneed a shared meal more frequently. Con-sequently, the sharing behavior in D. ecau-data probably represents an important sur-vival strategy for this species that gives therecipient a new opportunity to find prey tofeed on. The fact that even a pregnant fe-male regurgitated blood for a conspecificalso suggests that the cost to the donor ismuch less than the benefit to the recipient,similar to D. rotundus, where the donor loses the equivalent of 7 h of its time to the starvation point while the recipient gains18 h over its starvation point (Altringham,1996).

The kinship of the individuals we ob-served sharing food was unknown, howeverit is very possible they were related, as seenin D. rotundus that shared food with closerelatives and sometimes with unrelated indi-viduals, which had been roostmates formany years (Wilkinson, 1984). We expectthat individual D. ecaudata recognize eachother and donate food in a reciprocal way,similar to that observed in D. rotundus.Diphylla ecaudata appears to have a com-plex social structure, however, it could be very different from that D. rotundus be-cause D. ecaudata roost solitarily and donot congregate in large groups when thereare many individuals in a cave (Greenhall et al., 1984). In contrast, D. rotundus roostsin colonies of 20 to 100 bats (Greenhall et

316 Short Notes

al., 1983). Clearly, the social interactions ofD. ecaudata require additional study.

The pair formed by the adult female andthe juvenile male of D. ecaudata suggeststhat this sharing behavior is part of parentalcare in this species, similar to that observedin Desmodus (Wilkinson, 1987; Schmidt,1988; Kunz and Hood, 2000). These batscould be related, but is also possible thatthis female could be sharing food with a young that is not its own. This would besimilar behavior to that observed in Des-modus, where several females will jointlycare for their young and form stable socialgroups. This is an advantage to juvenilesless than 4–5 months old who rely entire-ly on their mothers, since if a mother dies or abandons its offspring, the young will be fed with regurgitated blood by other females in the colony (Schmidt et al.,1980).

The food sharing behavior in D. ecauda-ta occurred between adults, and adults andjuveniles. It occurred also between females,and females and males. Although we did not find this behavior between males of anyage, we expect they perform this behaviortoo similar to that seen in Desmodus bats(Wilkinson, 1984; Denault and MacFarlane,1995).

Although the observations described inthis paper provide the first documentationof food sharing in D. ecaudata, the resultsare not surprising because of their diet.Food sharing behavior in Diphylla requiresfurther study to provide a better understand-ing of the many aspects this behavior and itrelation to Diphylla’s social system. Our ob-servations also raise questions regarding thesimilarity of this species with Desmodus ro-tundus. For example, how often do D. ecau-data fail to find a prey and what is theweight lost rate of D. ecaudata prior to star-vation? Also, do vampire bats solicit bloodfrom more than one donor in the samenight?

As far as we know, this sharing behav-ior has yet to be observed for Diaemusyoungii, the third species of vampire bat(Uieda, 1992, 1993, 1996; Uieda et al.,1992; Greenhall and Schutt, 1996). We sus-pect it is very possible that they perform thisaltruism similar to that in Desmodus andDiphylla and also deserves study to help usincrease our understanding of this behaviorin this group of bats.

ACKNOWLEDGMENTS

We are grateful to Rocío Cruz-García and RicardoRangel-Martinez for their friendship and hard workduring field activities. To María Luisa Franco Mora-les, María de Jesús Teniente Franco and Dr. WilsonUieda who provided some bibliographic materialused in this manuscript. To Dr. Wies³aw Bogdano-wicz and five anonymous referees for their valu-able comments that improved this manuscript. Thisstudy was supported by the General Graduate Co-ordination and Research of the National PolythecnicInstitute (990210 y 200506), México D.F. This is a contribution to the Program for Conservation ofMexican Bats (PCMM), Bioconciencia, and WildlifeTrust.

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ELIZALDE-ARELLANO, C. 2003. Aspectos reproduc-tivos y de historia de vida del vampiro Diphyllaecaudata (Mammalia, Chiroptera). M.Sc. Thesis,Universidad Nacional Autónoma de México, Mé-xico D.F., 129 pp.

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MEDELLÍN, R. A., and W. LÓPEZ-FORMENT. 1986. Lascuevas, un recurso compartido. Anales del Insti-tuto de Biología, Universidad Nacional Autono-ma de México, Serie Zoológica, 56: 1027–1034.

MILLS, R., 1980. Parturition and social interactionamong captive vampire bats, Desmodus rotundus.Journal of Mammalogy, 61: 336–337.

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Received 18 September 2006, accepted 28 January 2007

First record of seasonal over sea migration of Miniopterus schreibersiiand Myotis capaccinii between Balearic Islands (Spain)

BLANCA AMENGUAL, MARC LÓPEZ-ROIG, and JORDI SERRA-COBO

Science Group Research of Biology of Vertebrates (96-SGR0072), Departament de Biologia Animal, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 645, 08028 Barcelona, Spain

E-mail: serracobo@areambiental.com

Key words: Miniopterus schreibersii, Myotis capaccinii, seasonal displacement, over sea migration, Balearic Islands

INTRODUCTION

Temperate bats have different require-ments depending on the season of the year,a fact that causes many species to changerefuges. The Schreibers’ bat (Miniopterusschreibersii) and the long-fingered bat (My-otis capaccinii) are two regional migrant batspecies, with a relatively fast flight, whoseseasonal displacement distances vary wide-ly. These species move between warm sum-mer roosts, commonly located in areas richin food resources, and winter quarters,whose main features are high humidity andrather low and relatively constant tempera-tures (Serra-Cobo, 1990, 1992). Seasonalmovements of M. schreibersii are amongthe most studied in European bats (Balcells,1962; Heymer, 1964; Roer, 1967; Aellen,1983; Palmeirim and Rodrigues, 1995;Jeantet and Gory, 1997; Paunovic, 1997a,1997b, 1998; Gaisler et al., 2003). The av-erage length of distances covered verified

in north-east Spain, between winter andsummer shelters, is 120 km (Serra-Cobo et al., 1998). Seasonal displacements of M. capaccinii are little known. The fewstudies carried out indicate that this speciesmakes short distance movements (40–50km) between shelters (Paunovic, 1997a,1997b, 1998; Paunovic and Karapandza,1999). The longest documented distance forM. capaccinii is 140 km (Hutterer et al.,2005). However, even less is known to dateabout the displacements these species carryout on the sea. Previous studies have report-ed bat seasonal displacements over sea between Sweden and Germany, but only for long-distance migratory species such as Pipistrellus nathusii and Nyctalus noctula(Gerell, 1987; Meinig, 2004). Exchangesbetween bat colonies located in different is-lands of an archipelago have not been con-firmed, except in the Maltese archipelago,where distances between the islands areminimal (Hutterer et al., 2005). The present

320 Short Notes

FIG. 1. Displacements of M. capaccinii (broken line) and M. schreibersii (continuous line) between Menorca and Mallorca (Balearic Islands, Spain)

article brings forward the first citations onbat displacements between the BalearicIslands (Spain).

Miniopterus schreibersii and M. capac-cinii inhabit two of the four main islands of the Balearic archipelago: Mallorca andMenorca. In both islands it has been provedthat these two species usually share refuges,as it also happens in the Iberian Peninsula(Serra-Cobo and Balcells, 1987; Serra-Cobo, 1992). Only a winter refuge (Curt’scave) is known in Menorca for these twospecies. From December to February thiscavity sheltered the major part of M. schrei-bersii population in Menorca (some 2,200individuals) and a small group of M. ca-paccinii (less than 20 individuals). During winter 2005–2006, 104 (30XX, 74YY) M. schreibersii and six (3XX, 3YY) M. ca-paccinii were ringed in this refuge. From

mid-April to the end of summer the Ra-tapinyades cave in Mallorca is occupied bya maternity colony of a hundred individualsof M. schreibersii and around 50 M. ca-paccinii. A total of 25 (15XX, 10YY) and47 (11XX, 36YY) M. schreibersii and six(4XX, 2YY) and 20 (5XX, 15YY) M. ca-paccinii were ringed in spring 2000 and2003, respectively. No winter cave for M. schreibersii and M. capaccinii is knownin Mallorca to date. The linear distance be-tween Curt’s cave and Ratapinyades cave isabout 100 km. The distance between thecoasts of Mallorca and Menorca oscillatesbetween 40 and 51 km, approximately. Thedata obtained demonstrate that there is anexchange of bats between the islands andthat these displacements occur in both di-rections (Fig. 1). Two females of M. schrei-bersii ringed in breeding refuge on Mallorca

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were recaptured on Menorca during winters2000–2001 and 2003–2004, respectively.The female ringed in 2003 was recapturedin an autumn shelter (Can Sion cave) be-fore crossing the sea to Menorca. The samedisplacement but in the opposite directionwas carried out by a female of M. capacciniiringed on Menorca and recaptured on Ma-llorca in 2006 (Fig. 1). There is no evidencethat these bats return to the refuge wherethey were ringed. However, the high fideli-ty of bats to maternity and winter coloniessuggests that these returns are possible.Furthermore, M. capaccinii uses the samerefuges as M. schreibersii in Mallorca andMenorca with a coincidence in time andplace, which makes us think that the use ofmigratory routes may also be similar.

Our data provide evidence on the sea-sonal displacements of M. schreibersii andM. capaccinii between the islands of Ma-llorca and Menorca and show the capacity of the two species to orient themselves and cover distances of at least 40 km overthe sea. It has been observed that M. schrei-bersii uses landmarks to orient itself duringits seasonal displacements, such as riversand cliffs (Serra-Cobo et al., 2000). Minio-pterus schreibersii and M. capaccinii of the Balearic Islands are capable of flyingover the sea in the absence of landmarks. Inthis sense, the Earth’s magnetic field canplay an important role in their navigation, asit happens with other bat species (Holland et al., 2006).

The distance between Mallorca and Me-norca does not constitute a geographic bar-rier for these two species as it seems to befor Myotis myotis in Gibraltar Strait (Ca-stella et al., 2000). The possibility of an ex-change between individuals of both speciesfrom Mallorca and Menorca is an importantfactor to be taken into account in the epi-demiological studies being carried out onbat Lyssavirus (Serra-Cobo et al., 2002) and in the studies on population dynamics

of M. schreibersii and M. capaccinii. Addi-tionally, the existence of exchanges be-tween islands is a very important character-istic to be considered when taking measuresfor the conservation of these two species,since the actions carried out on one islandmay have consequences on the other.

ACKNOWLEDGEMENTS

We wish to acknowledge Josep Márquez, AuriRipoll, Marta Torres, Xavier Bayer and Cisco Guaschfor their cooperation in the field work. The Consel-leria de Medi Ambient (Govern de les Illes Balears)financed this study.

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Received 30 January 2007, accepted 13 March 2007