Diet, Reproduction and Roosting Habits of the Madagascar Free-Tailed Bat, Otomops Madagascariensis Dorst, 1953 (Chiroptera: Molossidae)

Acta Chiropterologica, 9(2): 445–450, 2007 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS

Diet, reproduction and roosting habits of the Madagascar free-tailed bat, Otomops madagascariensis Dorst, 1953 (Chiroptera: Molossidae)

DAUDET ANDRIAFIDISON1, 2, AMYOT KOFOKY1, 3, TSIBARA MBOHOAHY4, PAUL A. RACEY5, and RICHARD K. B. JENKINS1, 5, 6

1Madagasikara Voakajy, B.P. 5181, Antananarivo, Madagascar 2Département de Biologie Animale, Faculté des Sciences, Université d’Antananarivo, B.P. 906, Antananarivo, Madagascar 6Vahatra, B.P. 738, Antananarivo, Madagascar 4Département de Biologie Animale, Faculté des Sciences, Université de Toliara, B.P. 185 (601) Toliara, Madagascar 5School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, United Kingdom 6Corresponding author: E-mail: [email protected]

Otomops madagascariensis is a large (24–27 g) molossid bat endemic to Madagascar. Unlike its congener O. martiensseni, in nearby mainland Africa, little is known about its ecology although it appears to roost only in caves. It is only known from a few sites in the west and occupies a small percentage of the available caves. We studied roosting colonies in seven vertical erosion domes in the roof of a cave in Parc National Tsingy de Bemaraha during July and October 2003. We also captured bats as they emerged from and returned to a roost cave in the south. Female bats examined in the west during October and in the south during November were pregnant. In the roosting colonies, one group contained 57 pregnant females and five adult males. Most other groups also consisted of both sexes but three male-only groups were encountered in October. Diet consisted mainly of Lepidoptera and Coleoptera and there was variation between sites and study locations in the contribution of these prey types. Otomops madagascariensis is an obligate cave dweller that appears to be rare within its known range and should be a target species for conservation and research.

Key words: breeding, caves, Otomops, diet, Madagascar, Molossidae, reproduction

INTRODUCTION be associated with sites on limestone or sandstone where it roosts in caves (Good- Otomops madagascariensis is endemic man et al., 2005). Although O. martiensseni to Madagascar and is thought to be an obli- has been the subject of a number of studies gate cave-dweller, unlike the closely relat- (Mutere, 1973; Rydell and Yalden, 1997; ed Otomops martiensseni from the African Fenton et al., 2002, 2004), there are few mainland which forms colonies in houses data available on the biology of O. mada- (Fenton et al., 2002). The distribution of gascariensis. Here we report on the popula- O. madagascariensis covers western Mada- tion structure of O. madagascariensis from gascar, from north to south, and appears to sites in western and southern Madagascar 446 D. Andriafidison, A. Kofoky, T. Mbohoahy, P. A. Racey, and R. K. B. Jenkins and investigate patterns of seasonality in PN Tsingy de Bemaraha and Sarodrano food habits and reproduction. sites but males were significantly larger than females (in mm, 0 ± SE), 61.9 ± 0.15, MATERIALS AND METHODS and 60.9 ± 0.11, respectively (2-way ANOVA, site — F1, 421= 3.5, P >> 0.05, sex We studied roosting bats in Anjohikinakina cave — F1, 421 = 33.2, P < 0.001, interaction — (19°0.59’S, 44°46.06’E, 100 m a.s.l.) in the Parc Na- F1, 421 = 0.3, P >> 0.05). At PN Tsingy de tional (PN) Tsingy de Bemaraha, Province de Ma- Bemaraha, male and female body mass (in hajunga, between 12 and 15 August and 29 and 30 October 2003. Bats roosted in circular erosion domes g) differed significantly between seasons in the ceiling and we assigned numbers to individual (2-way ANOVA, sex — F1, 192 = 1.2, domes that were retained throughout the study. We P > 0.05, month — F1, 290 = 22.5, P < 0.001) used long-handled sweep nets to collect all roosting and increased between August (YY — individuals within each erosion dome. 25.6 ± 0.74, XX, 25.1 ± 0.33) and October At Namaza canyon on 29 April 2003, PN d’Isalo, Province de Fianarantsoa (22°32.4’S, 45°22.8’E, 800 (YY — 27.8 ± 0.38, XX — 27.3 ± 0.33). m a.s.l.) we trapped flying bats using a 12 m mist net At Sarodrano, both sex and month and the set over a small river. In the south of Madagascar, at interaction were significant factors (2-way Ambanalia cave near Sarodrano village, Province de ANOVA, sex — F1, 223= 4.5, P < 0.05, Toliara, bats were trapped using a 9-m mist net erect- month — F = 32.8, P < 0.001, interac- ed across a cave entrance. The captures were under- 2, 223 taken as bats left their cave roost on 15 June 2003 and tion — F2, 223 = 9.6, P < 0.01). Male body as they returned to it after foraging on 25 November mass was lower in February (23.0 ± 0.32) 2003 and 23 February 2004 (23°32.40’S, 43°44.76’, than in June (26.3 ± 0.62) or November 1 m a.s.l.). We were unable to enter the cave at Am- (26.8 ± 0.39). Females by contrast attained banilia because of local taboos. Bats were kept in lowest body mass in June (22.9 ± 0.63) and cloth bags for a short time in order to collect faeces for diet analysis. Each bat was weighed (Pesola bal- peaked in November (26.6 ± 0.41) before ance, nearest 0.5 g), measured (forearm, nearest mm) decreasing again in February (24.0 ± 0.31). and aged (adult or juvenile based on ossification of There were no pregnant females in August phalanges) and sexed before release. at PN Tsingy de Bemaraha, but 95% of the Bat faeces were stored in plastic vials with 70% 80 females were pregnant in October. At ethanol. Faecal pellets were teased apart with dissect- Sarodrano, no pregnancies were noted in ing needles, with the aid of a binocular microscope (10–20×) in a Petri dish. All potentially identifiable June and February but 45% of the 53 fe- arthropod remains were removed, mounted in glyc- males netted in November were pregnant. erin on a slide, sealed with nail varnish and examined In Sarodrano, 54% of the 28 captures in with a binocular microscope (40–400×). Identifica- June and 63% of the 67 captures in Novem- tion was achieved using generic keys for bat faeces ber were female. This pattern was similar to together with other keys and monographs on invertebrate morphology (Delvare and Alberlanc, 1989; Anjohikinakina cave where 54% of the 93 Scholtz and Holm, 1989). We visually estimated per- bats caught in August and 75% of the 106 centage volume of major prey types following the captures in October were female. At the lat- methods of Whitaker (1988). ter site, where we were able to trap all roosting individuals, the sex ratio (YY:XX) RESULTS changed from 1:1.1 in June to 1:3.1 in Oc- tober without a major change in colony size. In total, we captured 427 O. madagas- At PN Tsingy de Bemaraha we captur- cariensis during the study, 196 in PN Tsingy ed all individuals in each roosting group de Bemaraha, 229 at Sarodrano and two in and no other O. madagascariensis was PN d’Isalo. There was no significant differ- found in the cave. We sampled the same ence in forearm length between bats from seven roosting groups during the two study Biology of Otomops madagascariensis 447

TABLE 1. Summary of the population structure of of males varying from 11% to 95%. In Oc- O. madagascariensis from seven erosion domes used tober the composition of hole 1 changed as roosts in the ceiling of a cave in Parc National markedly to 82% female. Hole 7, which Tsingy de Bemaraha, Madagascar during August and October 2003 was unoccupied in July contained 62 bats in October, 92% of which were female. Small Roost Total holeMonth bats YY XX %YY numbers of males were found in holes 2–6 1 August 48 19 29 40 and only in hole 1 were males common October 22 4 18 18 (Table 1). All four holes with females in 2 August 19 2 17 11 October contained pregnant bats. October 1 1 0 100 Based on percentage volume, the diet of 3 August 19 18 1 95 O. madagascariensis is comprised mainly October 8 4 4 50 4 August 7 5 2 71 of Coleoptera and Lepidoptera with other October 7 6 1 86 orders making a minor contribution (Table 5 August 00002). There were few differences in diet be- October 3 3 0 100 tween the sexes although the percentage 6 August 0000volume of dipterans was significantly high- October 3 3 0 100 7 August 0000er in female diet (Table 2). In PN Tsingy de October 62 5 57 8 Bemaraha, Lepidoptera and Coleoptera were the most common prey items by vol- periods, ranging in size from 7 to 48 indi- ume, but Diptera were also important in viduals in August and 1 to 62 individuals in October (Table 3). Seasonal differences October (Table 1). The erosion domes in were more pronounced from Sarodrano in which the bats were roosting were approxi- southern Madagascar, with most Coleoptera mately 15–20 m from the ground. All seven in the faeces during February and Lepido- erosion domes were occupied by bats in ptera in November (Table 3). October but only four were occupied Au- gust. In August, the sex ratio was almost DISCUSSION equal, with 47% males and 53% females but it was more female-biased in October All known roosts of O. madagascarien- with only 33% males (Table 1). sis are inside caves, with colonies reported In August, roosting groups consisted of from Sarodrano, PN Tsingy de Bemaraha mostly males in holes 3 and 4, whilst fe- and RS Ankarana (Cardiff, 2006; Kofoky et males were most numerous in holes 1 and 2. al., 2007). Otomops martiensseni usually During this month, all four occupied holes roosts in caves in East Africa (Kingdon, had males and females with the percentage 1974) but frequently uses houses in South

TABLE 2. The percentage volume (0 ± SE) of six invertebrate orders in the diet of 22 males and 33 females of O. madagascariensis from Madagascar. F-values and significance are given for ANOVAs on arcsine transformed percentages Order All bats YY XX F-value Lepidoptera 43.5 ± 3.37 44.3 ± 3.77 42.9 ± 5.06 0.58 Coleoptera 38.9 ± 2.86 40.1 ± 3.77 38.1 ± 2.86 0.07 Diptera 5.5 ± 1.06 2.4 ± 1.07 7.5 ± 1.53 6.10* Hemiptera 3.3 ± 1.25 4.4 ± 2.18 2.6 ± 1.51 0.50 Heteroptera 1.50 ± 0.76 1.52 ± 0.89 1.36 ± 1.36 0.16 Ephemeroptera 1.2 ± 0.84 0.00 1.9 ± 1.39 1.27 * — P < 0.05 448 D. Andriafidison, A. Kofoky, T. Mbohoahy, P. A. Racey, and R. K. B. Jenkins

TABLE 3. The percentage volume (0 ± SE) of six invertebrate orders in the diet of O. madagascariensis from two sites during different seasons. Number of individual bats in parentheses PN Tsingy de Bemaraha Sarodrano Order October (11) August (14) February (13) November (15) Lepidoptera 31.0 ± 4.60 41.1 ± 4.55 28.5 ± 5.86 72.6 ± 3.30 Coleoptera 44.2 ± 4.58 42.8 ± 4.67 48.3 ± 6.50 19.9 ± 2.97 Diptera 15.2 ± 3.30 2.6 ± 1.35 2.4 ± 1.07 2.5 ± 0.62 Hemiptera 0.9 ± 0.91 3.2 ± 1.45 9.8 ± 4.64 0.0 Heteroptera 3.6 ± 2.53 2.4 ± 2.14 0.0 0.7 ± 0.54 Ephemeroptera 0.0 0.0 4.9 ± 3.45 0.0

Africa (Fenton et al., 2002). Other members 57 pregnant females and 5 males, giving of the genus are hole and cavity roosting a ratio of 1 male to 11 females, which is bats (e.g., Ramakrishna et al., 2003). similar to the reported sex ratio of O. mar- There is little published information on tiensseni (Fenton et al., 2002). Male-only the roosting ecology of O. madagascarien- groups present during October were pre- sis although Cardiff (2006) reported a pref- sumably unattached ‘bachelor’ males. The erence for caves with a large entrance relative size and suitability of each erosion and high ceiling in northern Madagascar. In dome may determine the breeding system. a survey of O. martiensseni roosts in Dur- As Fenton et al. (2002) studied O. mar- ban, Fenton et al. (2002) reported a mean tiensseni in January, when females were colony size of 11.2 individuals from 24 at- lactating, further studies on O. madagas- tics. However, in caves in coastal Kenya cariensis are needed especially as another Mutere (1973) captured between 20 and 848 roosting colony in PN Tsingy de Bemaraha, bats per year from two caves indicating that in a cave near Antsalova (R. K. B. Jenkins, O. martiensseni roosts in colonies of vari- personal observations), appears to have a ous sizes, which may be determined by the different roosting formation, consisting of a volume of the cavity. In their five study single group of 100–300 individuals sur- colonies, only 6 of 84 bats were adult males rounded by satellite groups in circular de- and a male with a well-developed gular pressions in the cave roof. gland occupied each building (Fenton et al., Mutere (1973) recorded peak male testis 2002). This harem organization may also be mass in August just before the onset of present in larger roosting aggregations but pregnancy in females. We were unable to may be more difficult for biologists to de- follow the breeding condition of a single tect (Fenton et al., 2002). There was no di- colony but pregnancy was noted in October rect evidence of a harem mating system in and November in western and southern our study cave because no roosting group Madagascar respectively. Differences in the consisted of a single large male with fe- proportion of pregnant females between males and sub-adults. In August most males sites could be attributed to the difference in were found in two erosion domes, both of the timing of breeding between latitudes. which contained females. Erosion domes Another possibility is that as we trapped 1 and 2 contained 19 and 18 males respec- bats leaving the roosts in the south but cap- tively but corresponding female numbers tured bats inside the roost in the west, our 29 and 1. In October, when most of the fe- results may have been influenced by the be- males were obviously pregnant, three haviour and activity patterns of pregnant fe- domes contained only males and another six males, as only active bats were sampled males and a female. One dome contained from Sarodrano. Biology of Otomops madagascariensis 449

Increases in female body mass between abundance of caves, only a few were found the austral winter (June and August) and the to contain roosting O. madagascariensis austral summer (October and November) (Cardiff, 2006; Kofoky et al., 2007). There- are associated with pregnancy. There was fore, as an obligate cave species, known no clear pattern of male mass change during from only a small proportion of caves that the same periods but this may be associated have been surveyed for bats, the conserva- with breeding status. In a harem system, the tion status of O. madagascariensis will de- energy budget of harem masters (i.e. those pend on the degree of protection afforded to that control access to groups of females) is these caves. likely to be different to subordinate males. As large bodied bats with narrow wings, ACKNOWLEDGEMENTS Otomops typically fly high and fast and take flying insects on the wing. Studies on We thank the Direction des Eaux et Forêt and Association Nationale pour la Gestion des Aires O. martiensseni have shown it forages at Protégées for permission to conduct the work. We are least 3 km from roosts (Fenton et al., 2002) especially grateful to the funders of this work: the and feeds almost exclusively on large moths Darwin Initiative (#162/10/024), National Geograph- (Rydell and Yalden, 1997). Otomops mada- ic Society (#C23-02), Rufford Small Grants, Bat gascariensis fed mostly on Coleoptera and Conservation International and the British Ecological Society (#2159). We also thank our partners, Pro- Lepidoptera but seasonal variation was evi- gramme Bemaraha, Association Nationale pour la dent from both study sites, particularly for Gestion des Airees Protégées, the Département de the latter order. Kingdon (1974) and Mutere Biologie Animale, Faculté des Sciences, Université (1973) suggest that O. martiensseni mi- d’Antananarivo and the Faculté des Sciences, Uni- grates during periods of food shortage, al- versité de Toliara and. In particular we’d like to thank Hery Lala Ravelomanantsoa, Olga Ramilijaona, Dan- though there is at present no evidence of iel Rakotondravony and Felicité Rejo-Fienena for this from Madagascar. However, major their support. Numerous guides assisted us in the field changes to the proportion of males and fe- as well as our colleagues Fanja Ratrimomanarivo, males at Anjohikinakina cave between Radosoa Andrianaivoarivelo and Félicien Randrian- andrianina. Jon Russ and two anonymous referees August and October points to seasonal provided helpful comments on an earlier version of movements and the existence of other the manuscript. colonies. Such movements are likely to de- pend on the local availability of prey and in LITERATURE CITED Madagascar this may vary according to ge- ographical region. The diet of three other ANDRIANAIVOARIVELO, R. A., N. RANAIVOSON, P. A. Malagasy molossids is made up predomi- RACEY, and R. K. B. JENKINS. 2006. The diet of three synanthropic bats (Chiroptera: Molossidae) nantly of Lepidoptera and Hemiptera, with from eastern Madagascar. Acta Chiropterologica, Diptera and Coleoptera important seasonal- 8: 439–444. ly (Andrianaivoarivelo et al., 2006). How- CARDIFF, S. G. 2006. Bat cave selection and conser- ever, this study was conducted in the humid vation in Ankarana, northern Madagascar. MSci. east of Madagascar and little is known Thesis, Columbia University, New York, 73 pp. DELVARE, G., and H. P. ABERLANC. 1989. Les insectes about the diet of the molossid species that d’Afrique et d’Amérique-Tropicale. Clés pour la occur sympatrically with O. madagasca- reconnaissance des familles. CIRAD (Centre de riensis. Coopération Internationale en Recherche Agro- Otomops madagascariensis was found nomique pour le Développement), Montpellier, in seven of the 13 sites surveyed recent- 302 pp. FENTON, M. B., P. J. TAYLOR, D. S. JACOBS, E. J. ly in western Madagascar (Goodman et RICHARDSON, E. BERNARD, S. BOUCHARD, K. R. al., 2005). In two of these, despite an DEBAEREMAEKER, H. TER HOFSTEDE, L. HOLLIS, 450 D. Andriafidison, A. Kofoky, T. Mbohoahy, P. A. Racey, and R. K. B. Jenkins

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Received 04 August 2007, accepted 16 November 2007