https://doi.org/10.4081/tz.2020.68
Timing of emergence and cave return, and duration of nocturnal activity in an endemic Malagasy fruit bat
Submitted: 19 April 2020
Accepted: 18 May 2020
Published: 11 June 2020
Accepted: 18 May 2020
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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Bats emerge from their day roost after dusk and different factors can affect the timing of departure, return, and duration of nocturnal activities. This study provides information on the time of emergence and return of an endemic Malagasy fruit bat, Rousettus madagascariensis, in a cave located in the Réserve Spéciale d’Ankarana, northern Madagascar. Individuals were captured in a narrow passage between the roost and cave exit and capture time for each individual was noted. Variation according to sex, age, and body condition, as well as the influence of season, and the sunset and sunrise time were analyzed. During the dry season, individuals started to emerge at 1913 hours and returned to the cave generally by 0505 hours; the duration of time outside the cave during the dry season was higher in adult females (0952 hours) followed by subadult males (0937 hours), sub-adult females (0931 hours), and adult males (0910 hours). During the wet season, individuals exited at 1926 hours and returned at 0351 hours; as in the dry season, adult females spent more time outside the cave (0833 hours), than sub-adult females (0800 hours), and adult males (0752 hours). The period of emergence varied according to the age and sex classes, and time of predawn return associated with the previous nocturnal activity. The period of return was influenced by season, and age and sex classes. Such information is useful to quantify shifts in bat ecology, especially for endemic species with limited distribution or those playing an important role in ecosystem services.
Acharya PR, Racey PA, McNeil D, Sotthibandhu S, Bumrungsri S. 2015. Timing of cave emergence and return in the dawn bat (Eonycteris spelaea, Chiroptera: Pteropodidae) in southern Thailand. Mammal Study. 40(1):47–52.
DOI: https://doi.org/10.3106/041.040.0108
Altringham JD. 1996. Bats: Biology and behaviour. New York: Oxford University Press. 278 pp.
Andriafidison D, Andrianaivoarivelo RA, Ramilijaona OR, Razanahoera MR, MacKinnon J, Jenkins RKB, Racey PA. 2006. Nectarivory by endemic Malagasy fruit bats during the dry season. Biotropica. 38(1):85–90.
Andrianaivoarivelo RA. 2012. Ecologie et population de Rousettus madagascariensis G. Grandidier, 1928 (Pteropodidae). Unpublished PhD Thesis. Universités de Rennes 1 et d’Antananarivo, Rennes. 162 pp.
Andrianaivoarivelo RA, Ramilijaona O, Racey PA, Razafindrakoto N, Jenkins RKB. 2011. Feeding ecology, habitat use and reproduction of Rousettus madagascariensis Grandidier, 1928 (Chiroptera: Pteropodidae) in eastern Madagascar. Mammalia. 75(1):69–78.
DOI: https://doi.org/10.1515/mamm.2010.071
Anthony ELP. 1988. Age determination in bats. In: Kunz TH, editor. Ecological and behavioral methods for the study of bats. Washington, D.C.: Smithsonian Institution Press. p. 47–58.
Appel G, López-Baucells A, Magnusson WE, Bobrowiec PED. 2019. Temperature, rainfall, and moonlight intensity effects on activity of tropical insectivorous bats. Journal of Mammalogy. 100(6):1889–1900.
Bachorec E, Horáček I, Hulva P, Konečný A, Lučan RK, Jedlička P, Shohdi WM, Řeřucha Š, Abi-Said M, Bartonička T. 2020. Spatial networks differ when food supply changes: Foraging strategy of Egyptian fruit bats. PLoS ONE. 15(2):e0229110.
DOI: https://doi.org/10.1371/journal.pone.0229110
Balasingh J, Koilraj J, Kunz TH. 1995. Tent construction by the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae) in southern India. Ethology. 100(3):210–229.
DOI: https://doi.org/10.1111/j.1439-0310.1995.tb00326.x
Barclay RMR, Jacobs DS. 2011. Differences in the foraging behaviour of male and female Egyptian fruit bats (Rousettus aegyptiacus). Canadian Journal of Zoology. 89(6):466–473.
DOI: https://doi.org/10.1139/z11-013
Bullock DJ, Combes BA, Eales LA, Pritchard JS. 1987. Analysis of the timing and pattern of emergence of the pipistrelle bat (Pipistrellus pipistrettus). Journal of Zoology. 211(2):267–274.
Campbell P. 2008. The relationship between roosting ecology and degree of polygyny in harem-forming bats: Perspectives from Cynopterus. Journal of Mammalogy. 89(6):1351–1360.
DOI: https://doi.org/10.1644/08-MAMM-S-059.1
Cardiff SG, Befourouack J. 2008. La Réserve spéciale de l’Ankarana. In: Goodman SM, editor. Paysage naturels et biodiversité de Madagascar. Paris: Publications scientifiques du Muséum. p. 571–584.
Cawten L. 2014. Anti-predation strategies of chocolate wattked bats (Chalinolobus morio) after a predation event at a maternal roost by a southern boobook (Tyto novaeseelandiae). The Tasmanian Naturalist. 136:35–42.
Chaverri G, Kunz TH. 2010. Ecological determinants of social systems: Perspectives on the functional role of roosting ecology in the social behavior of tent-roosting bats. In: Macedo R, editor. Advances in the study of behavior. Cambridge: Academic Press. p. 275–318. http://www.sciencedirect.com/science/article/pii/S0065345410420094
DOI: https://doi.org/10.1016/S0065-3454(10)42009-4
Desmarest A.-G. 1820. Mammalogie, ou, description des espèces de mammifères. Paris: Mme. Veuve Agasse, imprimeur-libraire. 584 pp. https://www.biodiversitylibrary.org/bibliography/59887
DOI: https://doi.org/10.5962/bhl.title.59887
Dobson GE. 1871. Description of four new species of Malayan bats, from the collection of Dr. Stoliczka. The Journal of the Asiatic Society of Bengal. 40:260–267.
Downs CT, Zungu MM, Brown M. 2012. Seasonal effects on thermoregulatory abilities of the Wahlberg’s epauletted fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal, South Africa. Journal of Thermal Biology. 37(2):144–150.
DOI: https://doi.org/10.1016/j.jtherbio.2011.12.003
Ebensperger LA, Hurtado MJ. 2005. Seasonal changes in the time budget of degus, Octodon degus. Behaviour. 142(1):91–112.
Elangovan V, Marimuthu G. 2001. Effect of moonlight on the foraging behaviour of a megachiropteran bat Cynopterus sphinx. Journal of Zoology. 253(3):347–350.
Erkert HG. 1978. Sunset-related timing of flight activity in Neotropical bats. Oecologia. 37(1):59–67.
DOI: https://doi.org/10.1007/BF00349991
Erkert HG. 2000. Bats — Flying nocturnal mammals. In: Halle S, Stenseth NC, editors. Activity patterns in small mammals: An ecological approach. Berlin: Springer. p. 253–272. https://doi.org/10.1007/978-3-642-18264-8_16
DOI: https://doi.org/10.1007/978-3-642-18264-8_16
Fenton MB, Fleming TH. 1976. Ecological interactions between bats and nocturnal birds. Biotropica. 8(2):104–110.
DOI: https://doi.org/10.2307/2989629
Fleming TH. 1979. Do tropical frugivores compete for food? American Zoologist. 19(4):1157–1172.
DOI: https://doi.org/10.1093/icb/19.4.1157
Fleming TH, Heithaus ER. 1981. Frugivorous bats, seed shadows, and the structure of tropical forests. Biotropica. 13(2):45–53.
DOI: https://doi.org/10.2307/2388069
Garbino GST, Rezende GC, Tavares VDC. 2018. Tent use by Artibeus and Uroderma (Chiroptera, Phyllostomidae) in northern Colombia. Mastozoologia Neotropical. 25(2):467–472.
DOI: https://doi.org/10.31687/saremMN.18.25.2.0.08
García CB, García J, Martín MML, Salmerón R. 2015. Collinearity: Revisiting the variance inflation factor in ridge regression. Journal of Applied Statistics. 42(3):648–661.
DOI: https://doi.org/10.1080/02664763.2014.980789
Garg KM, Chattopadhyay B, Ramakrishnan U. 2018. Social structure of the harem-forming promiscuous fruit bat, Cynopterus sphinx, is the harem truly important? Royal Society Open Science. 5(2):172024.
Gehrt SD, Chelsvig JE. 2003. Bat activity in an urban landscape: Patterns at the landscape and microhabitat scale. In: Marzluff JM, Shulenberger E, Endlicher W, Alberti M, Bradley G, Ryan C, Simon U, ZumBrunnen C, editors. Urban ecology: An international perspective on the interaction between humans and nature. Boston, MA: Springer US. p. 437–453. https://doi.org/10.1007/978-0-387-73412-5_29
DOI: https://doi.org/10.1007/978-0-387-73412-5_29
Geoffroy ES-H. 1810. Description des roussettes et des céphalotes, deux nouveaux genres de la famille des chauves-souris. Annales du Muséum d’Histoire Naturelle. 15:86–108.
Geoffroy ES-H. 1824. La physiologie animale et végétale, l’anatomie comparée des deux règnes, la zoologie, la botanique, la minéralogie et la géologie. Annales des Sciences Naturelles. 1:342–343.
Gittleman JL, Thompson SD. 1988. Energy allocation in mammalian reproduction. American Zoologist. 28(3):863–875.
DOI: https://doi.org/10.1093/icb/28.3.863
Gonsalves L, Bicknell B, Law B, Webb C, Monamy V. 2013. Mosquito consumption by insectivorous bats: does size matter? PLoS ONE. 8(10):e77183.
DOI: https://doi.org/10.1371/journal.pone.0077183
Goodman SM. 2011. Les chauves-souris de Madagascar. Antananarivo: Association Vahatra. 127 pp.
Goodman SM, Griffiths O. 2006. A case of exceptionally high predation levels of Rousettus madagascariensis by Tyto alba (Aves: Tytonidae) in western Madagascar. Acta Chiropterologica. 8(2):553–556.
DOI: https://doi.org/10.3161/1733-5329(2006)8[553:ACOEHP]2.0.CO;2
Goodman SM, Ramasindrazana B. 2018. Systématique des chauves-souris malgaches (ordre des Chiroptera) / Systematics of Malagasy bats (order Chiroptera). In: Goodman SM, Raherilalao MJ, Wohlhauser S, editors. Les aires protégées terrestres de Madagascar : Leur histoire, description et biote / The terrestrial protected areas of Madagascar: Their history, description, and biota. Antananarivo: Association Vahatra. p. 382–394.
Goodman SM, Rajemison FI, Noroalintseheno Lalarivoniaina OS. 2017. Morphometric patterns of secondary sexual dimorphism and seasonal differences in Rousettus madagascariensis from northern Madagascar. Acta Chiropterologica. 19(1):71–75.
DOI: https://doi.org/10.3161/15081109ACC2017.19.1.005
Goodman SM, Raherilalao MJ, Wohlhauser S, editors. 2018. Les aires protégées terrestres de Madagascar : Leur histoire, description et biote / The terrestrial protected areas of Madagascar: Their history, description, and biota. Antananarivo: Association Vahatra. 1716 pp
Grandidier G. 1928. Description de deux nouveaux mammifères insectivores de Madagascar. Bulletin du Muséum national d’Histoire Naturelle. 34:63–70.
Gray JE. 1821. On the natural arrangement of vertebrose animals. London Medical Repository. 15(1):296–310.
Hodgkison R, Balding ST, Akbar Z, Kunz TH. 2003. Roosting ecology and social organization of the spotted-winged fruit bat, Balionycteris maculata (Chiroptera: Pteropodidae), in a Malaysian lowland dipterocarp forest. Journal of Tropical Ecology. 19(6):667–676.
DOI: https://doi.org/10.1017/S0266467403006060
Kimura K, Waki H. 2017. Minimization of Akaike’s information criterion in linear regression analysis via mixed integer nonlinear program. Optimization Methods and Software. 33(3):633–649.
DOI: https://doi.org/10.1080/10556788.2017.1333611
Korine C, Arad Z. 1999. Changes in milk composition of the Egyptian Fruit Bat, Rousettus aegyptiacus (Pteropodidae), during lactation. Journal of Mammalogy. 80(1):53–59.
DOI: https://doi.org/10.2307/1383207
Korine C, Izhaki I, Makin D. 1994. Population structure and emergence order in the fruit-bat (Rousettus aegyptiacus: Mammalia, Chiroptera). Journal of Zoology. 232(1):163–174.
DOI: https://doi.org/10.1111/j.1469-7998.1994.tb01566.x
Korine C, Zinder O, Arad Z. 1999. Diurnal and seasonal changes in blood composition of the free-living Egyptian fruit bat (Rousettus aegyptiacus). Journal of Comparative Physiology B. 169(4):280–286.
Kunz TH. 1974. Feeding ecology of a temperate insectivorous bat (Myotis velifer). Ecology. 55(4):693–711.
DOI: https://doi.org/10.2307/1934408
Kunz TH, Anthony ELP. 1996. Variation in the timing of nightly emergence behavior in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae). In: Contributions in Mammalogy: A memorial volume honoring Dr J Knox Jones, Jr. Texas: Museum of Texas Tech University. p. 225–235.
Lee YF, McCracken GF. 2001. Timing and variation in the emergence and return of Mexican free-tailed Bats, Tadarida brasiliensis mexicana. Zoological Studies. 40(4):309–316.
Lučan RK, Bartonička T, Jedlička P, Řeřucha Š, Šálek M, Čížek M, Nicolaou H, Horáček I. 2016. Spatial activity and feeding ecology of the endangered northern population of the Egyptian fruit bat (Rousettus aegyptiacus). Journal of Mammalogy. 97(3):815–822.
DOI: https://doi.org/10.1093/jmammal/gyw014
Maier C. 1992. Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in Oxfordshire. Journal of Zoology. 228(1):69–80.
Marimuthu G, Rajan KE, Koilraj AJ, Isaac SS, Balasingh J. 1998. Observations on the foraging behavior of a tent roosting megachiropteran bat Cynopterus sphinx. Biotropica. 30(2):321–324.
DOI: https://doi.org/10.1111/j.1744-7429.1998.tb00066.x
Matschie P. 1899. Die fledermäuse des Berliner Museums für Naturkunde, vol. 1: Die Megachiroptera des Berliner Museums für Naturkunde. Berlin: Berliner Museums für Naturkunde. 118 pp.
DOI: https://doi.org/10.1515/9783111622965
McAney CM, Fairley JS. 1988. Activity patterns of the lesser horseshoe bat Rhinolophus hipposideros at summer roosts. Journal of Zoology. 216(2):325–338.
Molina GI. 1782. Saggio sulla storia naturale del Chile. Bologna: Aquino. 368 pp.
DOI: https://doi.org/10.5962/bhl.title.62689
Noroalintseheno Lalarivoniaina OS, Rajemison FI, Goodman SM. 2017. Survie et variation temporelle de la taille de la population de Rousettus madagascariensis (Chiroptera: Pteropodidae) de la Grotte des Chauves-sours d’Ankarana, nord de Madagascar. Malagasy Nature. 12:68–77.
Noroalintseheno Lalarivoniaina OS, Rajemison FI, Andrianarimisa A, Goodman SM. 2018. Variation saisonnière de la structure d’âge et de la sex-ratio de la population de Rousettus madagascariensis (Yinpterochiroptera : Pteropodidae) à Ankarana, nord de Madagascar. Revue d’Ecologie (Terre et Vie). 73(1):23–30.
Olsson A, Emmett D, Henson D, Fanning E. 2006. Activity patterns and abundance of microchiropteran bats at a cave roost in south-west Madagascar. African Journal of Ecology. 44(3):401–403.
DOI: https://doi.org/10.1111/j.1365-2028.2006.00661.x
Ortega J, Arita HT. 2000. Defence of females by dominant males of Artibeus jamaicensis (Chiroptera: Phyllostomidae). Ethology. 106:395–407.
DOI: https://doi.org/10.1046/j.1439-0310.2000.00557.x
Ramanantsalama RV, Noroalintseheno Lalarivoniaina OS, Raselimanana AP, Goodman SM. 2019. Seasonal variation in diurnal cave-roosting behavior of a Malagasy fruit bat (Rousettus madagascariensis, Chiroptera: Pteropodidae). Acta Chiropterologica. 21(1):115–127.
DOI: https://doi.org/10.3161/15081109ACC2019.21.1.009
Ramanantsalama RV, Noroalintseheno Lalarivoniaina OS, Raselimanana AP, Goodman SM. (in preparation). Influence of environmental parameters on the breeding of an endemic Malagasy fruit bat, Rousettus madagascariensis (Pteropodidae). Acta Chiropterologica.
Reher S, Ehlers J, Rabarison H, Dausmann KH. 2018. Short and hyperthermic torpor responses in the Malagasy bat Macronycteris commersoni reveal a broader hypometabolic scope in heterotherms. Journal of Comparative Physiology B. 188(6):1015–1027.
Ripperger SP, Kalko EKV, Rodríguez-Herrera B, Mayer F, Tschapka M. 2015. Frugivorous bats maintain functional habitat connectivity in agricultural landscapes but rely strongly on natural forest fragments. PLoS One. 10(4). e0120535. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4382216/
DOI: https://doi.org/10.1371/journal.pone.0120535
Roy K, Saha GK, Mazumdar S. 2020. Seasonal influence on the diurnal roosting behaviour of free-ranging Indian flying fox Pteropus giganteus in an urban landscape, India. Biologia. https://doi.org/10.2478/s11756-020-00472-4
DOI: https://doi.org/10.2478/s11756-020-00472-4
Rydell J, Speakman JR. 1995. Evolution of nocturnality in bats: Potential competitors and predators during their early history. Biological Journal of the Linnean Society. 54(2):183–191.
DOI: https://doi.org/10.1111/j.1095-8312.1995.tb01031.x
Schreber JCD. 1774. Die Säugthiere in Abbildungen nach der Natur, mit Beschreibungen. Erlangen: Expedition des Schreber’schen säugthier- und des Esper’schen Schmetterlingswerkes. 544 pp. https://www.biodiversitylibrary.org/bibliography/67399
DOI: https://doi.org/10.5962/bhl.title.67399
Scopoli GA. 1769. Anni Historico-Naturales. Leipzig: Library New York Botanical Garden. 151 pp.
Speakman JR. 1995. Chiropteran nocturnality. Symposia of the Zoological Society of London. 67:187–201.
Speakman JR, Racey PA. 1986. The influence of body condition on sexual development of male brown long-eared bats (Plecotus auritus) in the wild. Journal of Zoology. 210(4):515–525.
Speakman JR, Hays GC, Webb PI. 1994. Is hyperthermia a constraint on the diurnal activity of bats? Journal of Theoretical Biology. 171(3):325–339.
Stribna T, Romportl D, Demjanovič J, Vogeler A, Tschapka M, Benda P, Horáček I, Juste J, Goodman SM, Hulva P. 2019. Pan African phylogeography and palaeodistribution of rousettine fruit bats: Ecogeographic correlation with Pleistocene climate vegetation cycles. Journal of Biogeography. 46(10):2336–2349.
DOI: https://doi.org/10.1111/jbi.13651
Sugiura N. 1978. Further analysis of the data by Akaike’s information criterion and the finite corrections. Communications in Statistics - Theory and Methods. 7(1):13–26.
DOI: https://doi.org/10.1080/03610927808827599
Swift SM. 1980. Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in north-east Scotland. Journal of Zoology. 190(3):285–295.
Thies W, Kalko EKV, Schnitzler H-U. 2006. Influence of environment and resource availability on activity patterns of Carollia castanea (Phyllostomidae) in Panama. Journal of Mammalogy. 87(2):331–338.
DOI: https://doi.org/10.1644/05-MAMM-A-161R1.1
Thomas SP, Follette DB, Farabaugh AT. 1991. Influence of air temperature on ventilation rates and thermoregulation of a flying bat. American Journal of Physiology. 260(5):960–968.
Vahl M. 1797. Beskrivelse pa tre nye arter flagermuse. Skrifter Naturhistorie-Selskabet Copenhagen. 4:121–138.
Vanlalnghaka C, Joshi DS. 2005. Entrainment by different environmental stimuli in the frugivorous bats from the Lonar Crater. Biological Rhythm Research. 36(5):445–452.
DOI: https://doi.org/10.1080/09291010500287337
Vanlalnghaka C, Keny VL, Satralkar MK, Pujari PD, Joshi DS. 2005. Social entrainment in the old frugivorous bats, Rousettus leschenaulti from the Lonar Crater. Biological Rhythm Research. 36(5):453–461.
DOI: https://doi.org/10.1080/09291010500287568
Venables LSV. 1943. Observations at a pipistrelle bat roost. Journal of Animal Ecology. 12(1):19–26.
DOI: https://doi.org/10.2307/1409
Voigt CC, Lewanzik D. 2011. Trapped in the darkness of the night: Thermal and energetic constraints of daylight flight in bats. Proceedings of the Royal Society B. 278(1716):2311–2317.
Vololona J. 2020. Etude des interactions entre Rousettus madagascariensis G. Grandidier, 1928 (Chiroptera: Pteropodidae) et les plantes à fleurs de la Réserve Spéciale d’Ankarana, Nord de Madagascar. Approche palynologique. Unpublished PhD Thesis. Antananarivo: Université d’Antananarivo. 226 pp.
Vololona J, Ramavovololona P, Noroalintseheno Lalarivoniaina OS, Goodman SM. 2020. Fleurs visitées par Rousettus madagascariensis G. Grandidier, 1928 (Chiroptera : Pteropodidae) dans la Réserve Spéciale d’Ankarana, Madagascar. Bulletin de la Société Zoologique de France. 145(1):49–67.
Wakefield A, Stone EL, Jones G, Harris S. 2015. Light-emitting diode street lights reduce last-ditch evasive manoeuvres by moths to bat echolocation calls. Royal Society Open Science. 2(8):150291.
DOI: https://doi.org/10.1098/rsos.150291
How to Cite
Ramanantsalama, R. V. ., & Goodman, S. M. . (2020). Timing of emergence and cave return, and duration of nocturnal activity in an endemic Malagasy fruit bat. Tropical Zoology, 33(1). https://doi.org/10.4081/tz.2020.68
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