Bat flies: source of supplement nutrients for an endemic Malagasy fruit bat

Submitted: 25 February 2022
Accepted: 23 August 2022
Published: 20 October 2022
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Among frugivorous vertebrates, the nutritional composition of consumed fruits often needs supplementing by other food types, such as leaves, pollen or invertebrates, to meet dietary requirements. The endemic Malagasy fruit bat, Rousettus madagascariensis (Pteropodidae), actively feeds on their dipteran fly ectoparasites, principally of the family Nycteribiidae and Streblidae, during grooming activities. Since bat flies take blood meals from their hosts, the consumption of these flies by bats might represent a mechanism of recycling and reducing the loss of important nutritional components, such as minerals or proteins and fatty acids. The contribution of these ectoparasites to the diet of R. madagascariensis is 4–10% of the daily protein requirements. This is an important proportion for a species considered to be exclusively frugivorous.

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Aljane F, Ferchichi A. 2009. Postharvest chemical properties and mineral contents of some fig (Ficus carica L.) cultivars in Tunisia. Journal of Food, Agriculture and Environment. 7:209–212.
Allen ME, Ullrey DE. 2004. Relationships among nutrition and reproduction and relevance for wild animals. Zoo Biology. 23:475–487. DOI: https://doi.org/10.1002/zoo.20029
Andrianaivoarivelo RA, Ramilijaona OR, Racey PA, Razafindrakoto N, Jenkins RKB. 2011. Feeding ecology, habitat use and reproduction of Rousettus madagascariensis Grandidier, 1928 (Chiroptera: Pteropodidae) in eastern Madagascar. Mammalia. 75:69–78. DOI: https://doi.org/10.1515/mamm.2010.071
Andrianaivoarivelo RA, Jenkins RKB, Petit EJ, Ramilijaona O, Razafindrakoto N, Racey PA. 2012a. Rousettus madagascariensis (Chiroptera: Pteropodidae) shows a preference for native and commercially unimportant fruits. Endangered Species Research. 19:19–27. DOI: https://doi.org/10.3354/esr00441
Andrianaivoarivelo RA, Petit EJ, Razafindrakoto N, Racey PA. 2012b. Alimentation et dispersion de graines chez Rousettus madagascariensis G. Grandidier 1928, dans le Nord-ouest de Madagascar. Revue d’Ecologie (La Terre et La Vie). 67:179–191.
Baillon HE. 1895. Histoire naturelle des plantes. In Grandidier A, editor. Histoire physique, naturelle et politique de Madagascar. Paris, France: Imprimerie Nationale. p. 261–399.
Baker JG. 1885. Ficus (Urostigma) tiliaefolia. Journal of the Linnean Society, Botany. 21:443. DOI: https://doi.org/10.1111/j.1095-8339.1885.tb00549.x
Bedwal RS, Bahuguna A. 1994. Zinc, copper and selenium in reproduction. Experientia. 50:626–640. DOI: https://doi.org/10.1007/BF01952862
Berg CC. 1986. The Ficus species (Moraceae) of Madagascar and the Comoro Islands. Bulletin du Muséum National d’Histoire Naturelle Section B, Adansonia. 8:17–55.
Dempsey JL. 2004. Fruit bats: nutrition and dietary husbandry. In Bernard JB, Crissey S, Dierenfeld ES, Seyjagat J, Ullrey DE, editors. Nutrition Advisory Group Handbook Fact Sheet 014. p. 1–17. Available at: https://nagonline.net/wp-content/uploads/2014/01/NAG-FS014-FRUIT-BATS-AUG-2004.pdf
Dew JL, Boubli JP. 2005. Tropical fruits and frugivores: The search for strong interactors. Dordrecht, Netherlands: Springer. 260 pp. DOI: https://doi.org/10.1007/1-4020-3833-X
Dick CW, Patterson BD. 2006. Bat flies: Obligate ectoparasites of bats. In Morand S, Krasnov BR, Poulin R, editors. Micromammals and macroparasites. Tokyo: Springer. p. 179–194. DOI: https://doi.org/10.1007/978-4-431-36025-4_11
Donati G, Santini L, Eppley TM, Arrigo-Nelson SJ, Balestri M, Boinski S, Bollen A, Bridgeman LL, Campera M, Carrai V, et al. 2017. Low levels of fruit nitrogen as drivers for the evolution of Madagascar’s primate communities. Scientific Reports. 7:1–9. DOI: https://doi.org/10.1038/s41598-017-13906-y
Dumont ER, Weiblen GD, Winkelmann JR. 2004. Preferences of fig wasps and fruit bats for figs of functionally dioecious Ficus pungens. Journal of Tropical Ecology. 20:233–238. DOI: https://doi.org/10.1017/S0266467403001147
El-Mansi AA, Al-Kahtani MA, Abumandour MMA. 2019. Comparative phenotypic and structural adaptations of tongue and gastrointestinal tract in two bats having different feeding habits captured from Saudi Arabia: Egyptian fruit bat (Rousettus aegyptiacus) and Egyptian tomb bat (Taphozous perforatus). Zoologischer Anzeiger. 281:24–38. DOI: https://doi.org/10.1016/j.jcz.2019.05.005
Engriser EM. 1995. The effect of insect larvae infestation on fruit choice in phyllostomid fruit bats: An experimental study. Biotropica. 27:523. DOI: https://doi.org/10.2307/2388967
Feng Y, Chen XM, Zhao M, He Z, Sun L, Wang CY, Ding, WF. 2018. Edible insects in China: Utilization and prospects. Insect Science. 25:184–198. DOI: https://doi.org/10.1111/1744-7917.12449
Fleming TH, Breitwisch R, Whitesides GH. 1987. Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecology and Systematics. 18:91–109. DOI: https://doi.org/10.1146/annurev.es.18.110187.000515
Ganzhorn, JU, Arrigo-Nelson S, Boinski S, Bollen A, Carrai V, Derby A, Donati G, Koenig A, Kowalewski M, Lahann P, et al. 2009. Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS ONE. 4:e8253. DOI: https://doi.org/10.1371/journal.pone.0008253
Geoffroy ES-H. 1810. Description des Rousettes et des céphalotes, deux nouveaux genres de la famille des chauve-souris. Annales du Muséum d’Histoire Naturelle. 15:86–108.
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. 19:71–75. DOI: https://doi.org/10.3161/15081109ACC2017.19.1.005
Grandidier G. 1928. Description de deux nouveaux mammifères insectivores de Madagascar. Bulletin du Muséum National d’Histoire Naturelle. 34:63–70.
Gray JE. 1863. Description of some new species of Mammalia. Proceedings of the Zoological Society of London. p. 261–263.
Gunawan SH, Yazid NNA, Roslan A, Mohamed NZ, Abdullah MT. 2016. The role of frugivorous bats as seed dispersal agents of Kenyir forest area, Terengganu. Universiti Malaysia Terengganu International Annual Symposium on Sustainability Science and Management. p. 115–122.
Izhaki I, Safriel UN. 1989. Why are there so few exclusively frugivorous birds? Experiments on fruit digestibility. Oikos. 54:23. DOI: https://doi.org/10.2307/3565893
Jobling B. 1952. Description of two new species of Ascodipteron from Africa and one species of Nycteribosca from Madagascar (Diptera, Streblidae). Parasitology. 42:126–135. DOI: https://doi.org/10.1017/S0031182000084365
Korine C, Arad Z, Arieli A. 1996. Nitrogen and energy balance of the fruit bat Rousettus aegyptiacus on natural fruit diets. Physiological Zoology. 69:618–634. DOI: https://doi.org/10.1086/physzool.69.3.30164219
Kunth KS. 1817. Urticeae. In Humboldt FWHA and Bonpland AJA, editors. Nova Genera et Species Plantarum. Paris: Sumtibus Librairie Greco-Latino-Germanice. p. 28–50.
Lamarck J-B. 1788. Encyclopédie méthodique. Botanique. Paris: Panckoucke. 374 pp.
Lambert JE, Fellner V, McKenney E, Hartstone-Rose A. 2014. Binturong (Arctictis binturong) and kinkajou (Potos flavus) digestive strategy: Implications for interpreting frugivory in Carnivora and Primates. PLoS ONE. 9:e105415. DOI: https://doi.org/10.1371/journal.pone.0105415
Leach WE. 1821. The characters of seven genera of bats with foliaceous appendages to the nose. Transactions of the Linnean Society of London. 13:73–82. DOI: https://doi.org/10.1111/j.1095-8339.1821.tb00056.x
Linnaeus C. 1753. Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Tomus I & II. Stockholm: Impensis Laurentii Salvii. 1200 pp. DOI: https://doi.org/10.5962/bhl.title.59734
Linnaeus, C. 1758. Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Leipzig: Sumptibus Guilelmi Engelmann. 824 pp. DOI: https://doi.org/10.5962/bhl.title.542
Long E, Racey PA. 2007. An exotic plantation crop as a keystone resource for an endemic megachiropteran, Pteropus rufus, in Madagascar. Journal of Tropical Ecology. 23:397–407. DOI: https://doi.org/10.1017/S0266467407004178
Marshall AG. 1982. Ecology of insects ectoparasitic on bats. In Kunz TH, editor. Ecology of bats. Boston, USA: Springer. p. 369–401. DOI: https://doi.org/10.1007/978-1-4613-3421-7_10
Miller P. 1768. The gardeners dictionary, ed. 8. London, UK: Botanic Garden at Chelsea. 1513 pp.
Milton K, Dintzis FR. 1981. Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica. 13:177. DOI: https://doi.org/10.2307/2388122
Missouri Botanical Garden. 2017. Catalogue of the vascular plants of Madagascar. Tropicos. (accessed 27 January 2022).
Nasir A, Jaafar FI, Muhammad IU, Matazu KI, Yaradua AI, Usman A, Suleiman ZA, Sulaiman H, Nasir NM. 2020. Proximate and mineral composition of the fruit of Ficus polita. Journal of Applied Life Sciences International. 23:7–13. DOI: https://doi.org/10.9734/jalsi/2020/v23i830178
National Research Council. 2003. Nutrient requirements of non-human primates, 2nd edition. Washington, USA: The National Academies Press. 306 pp.
Obame-Nkoghe J, Rahola N, Bourgarel M, Yangari P, Prugnolle F, Maganga GD, Leroy EM, Fontenille D, Ayala D, Paupy C. 2016. Bat flies (Diptera: Nycteribiidae and Streblidae) infesting cave-dwelling bats in Gabon: Diversity, dynamics and potential role in Polychromophilus melanipherus transmission. Parasites and Vectors. 9:333. DOI: https://doi.org/10.1186/s13071-016-1625-z
Oleksy R, Racey PA, Jones G. 2015. High-resolution GPS tracking reveals habitat selection and the potential for long-distance seed dispersal by Madagascan flying foxes Pteropus rufus. Global Ecology and Conservation. 3:678–692. DOI: https://doi.org/10.1016/j.gecco.2015.02.012
Ortmann S, Bradley BJ, Stolter C, Ganzhorn JU. 2006. Estimating the quality and composition of wild animal diets–a critical survey of methods. In Hohmann G, Robbins MM, Boesch C, editors. Feeding ecology in apes and other primates. Ecological, physical, and behavioral aspects. Cambridge, UK: Cambridge University Press. p. 395–418.
Peters W. 1867. Über die Fiederhunde Pteropi und insbesondere über die Arten der Gattung Pteropus. Monatsberichte Der Königlichen Preussische Akademie Des Wissenschaften Zu Berlin. 865–872.
Picot M, Jenkins RKB, Ramilijaona O, Racey PA, Carrière SM. 2007. The feeding ecology of Eidolon dupreanum (Pteropodidae) in Eastern Madagascar. African Journal of Ecology. 45:645–650. DOI: https://doi.org/10.1111/j.1365-2028.2007.00788.x
Rajemison FI, Noroalintseheno Lalarivoniaina OS, Goodman SM. 2017a. Parasitism by Nycteribiidae and Streblidae flies (Diptera) of a Malagasy fruit bat (Pteropodidae): Effects of body size and throat gland development on parasite abundance. Journal of Medical Entomology. 54:805–811. DOI: https://doi.org/10.1093/jme/tjw245
Rajemison FI, Noroalintseheno Lalarivoniaina OS, Goodman, SM. 2017b. Bat flies (Diptera: Nycteribiidae, Streblidae) parasitising Rousettus madagascariensis (Chiroptera: Pteropodidae) in the Parc National d’Ankarana, Madagascar: Species diversity, rates of parasitism and sex ratios. African Entomology. 25:72–85. DOI: https://doi.org/10.4001/003.025.0072
Ramanantsalama RV, Andrianarimisa A, Raselimanana AP, Goodman SM. 2018. Rates of hematophagous ectoparasite consumption during grooming by an endemic Madagascar fruit bat. Parasites and Vectors. 11:330. DOI: https://doi.org/10.1186/s13071-018-2918-1
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. 21:115–127. DOI: https://doi.org/10.3161/15081109ACC2019.21.1.009
Ramanantsalama RV, Goodman SM, Dietrich M, Lebarbenchon C. 2022. Interaction between Old World fruit bats and humans: From large scale ecosystem services to zoonotic diseases. Acta Tropica. 231:106462. DOI: https://doi.org/10.1016/j.actatropica.2022.106462
Raubenheimer D, Rothman JM. 2013. Nutritional ecology of entomophagy in humans and other primates. Annual Review of Entomology. 58:141–160. DOI: https://doi.org/10.1146/annurev-ento-120710-100713
Raubenheimer D, Simpson SJ. 2018. Nutritional ecology and foraging theory. Current Opinion in Insect Science. 27:38–45. DOI: https://doi.org/10.1016/j.cois.2018.02.002
Raubenheimer D, Rothman JM, Pontzer H, Simpson SJ. 2014. Macronutrient contributions of insects to the diets of hunter-gatherers: A geometric analysis. Journal of Human Evolution. 71:70–76. DOI: https://doi.org/10.1016/j.jhevol.2014.02.007
Redford KH, Dorea JG. 1984. The nutritional value of invertebrates with emphasis on ants and termites as food for mammals. Journal of Zoology. 203:385–395. DOI: https://doi.org/10.1111/j.1469-7998.1984.tb02339.x
Redford KH, Bouchardet da Fonseca GA, Lacher TE. 1984. The relationship between frugivory and insectivory in primates. Primates. 25:433–440. DOI: https://doi.org/10.1007/BF02381666
Rothman JM, Raubenheimer D, Bryer MAH, Takahashi M, Gilbert CC. 2014. Nutritional contributions of insects to primate diets: Implications for primate evolution. Journal of Human Evolution. 71:59–69. DOI: https://doi.org/10.1016/j.jhevol.2014.02.016
Rumpold BA, Schlüter OK. 2013a. Nutritional composition and safety aspects of edible insects. Molecular Nutrition and Food Research. 57:802–823. DOI: https://doi.org/10.1002/mnfr.201200735
Rumpold BA, Schlüter OK. 2013b. Potential and challenges of insects as an innovative source for food and feed production. Innovative Food Science & Emerging Technologies. 17:1-11. DOI: https://doi.org/10.1016/j.ifset.2012.11.005
Seneviratne SS, Fernando HC, Udagama-Randeniya PV. 2009. Host specificity in bat ectoparasites: A natural experiment. International Journal for Parasitology. 39:995–1002. DOI: https://doi.org/10.1016/j.ijpara.2008.12.009
Tate GHH. 1942. Results of the Archbold expeditions. no. 46. A new genus and species of fruit bats, allied to Nyctimene. American Museum Novitates. 1204:1–2.
Tedman, RA, Hall LS. 1985. The morphology of the gastrointestinal tract and food transit time in the fruit bats Pteropus alecto and P. poliocephalus (Megachiroptera). Australian Journal of Zoology. 33:625–640. DOI: https://doi.org/10.1071/ZO9850625
Tendu A., Hughes AC, Berthet N, Wong G. 2022. Viral hyperparasitism in bat ectoparasites: Implications for pathogen maintenance and transmission. Microorganisms. 10:1230. DOI: https://doi.org/10.3390/microorganisms10061230
Terborgh J. 1992. Diversity and the tropical rain forest. New York:, USA Scientific American Library. 242 pp.
Theodor O. 1955. On the genus Eucampsipoda Kol. and Dipseliopoda n.g. Parasitology. 45:195–229. DOI: https://doi.org/10.1017/S0031182000027578
Thunberg CP. 1786. Dissertationes botanicae: D.d. Ficus genus. Uppsala: Apud Direct. Joh. Edman. 33 pp.
Tom-Dery D, Eller F, Jensen K, Reisdorff C. 2018. Effects of elevated carbon dioxide and climate change on biomass and nutritive value of Kyasuwa (Cenchrus pedicellatus Trin.). Journal of Applied Botany and Food Quality. 91:88–95.
Vahl MH. 1805. Ficus lutea Vahl. Enumeratio Plantarum. 2:185.
Valvi SR, Rathod VS. 2018. Mineral composition of some wild edible fruits from Kolhapur district. International Journal of Applied Biology and Pharmaceutical Technology. 2:392–396.
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. PhD Thesis. Université d’Antananarivo, Antananarivo. 257 pp.
Vololona J, Ramavovololona P, Goodman SM. 2020. Régime alimentaire de Rousettus madagascariensis (Chiroptera : Pteropodidae) dans la Réserve Spéciale d’Ankarana, nord de Madagascar. Bulletin de la Société Zoologique de France. 145:365–381.
Wagner I, Ganzhorn JU, Kalko EKV, Tschapka M. 2015. Cheating on the mutualistic contract: Nutritional gain through seed predation in the frugivorous bat Chiroderma villosum (Phyllostomidae). Journal of Experimental Biology. 218:1016–1021. DOI: https://doi.org/10.1242/jeb.114322
Wendeln MC, Runkle JR, Kalko EKV. 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica. 32:489–501. DOI: https://doi.org/10.1111/j.1744-7429.2000.tb00495.x
Wilkinson DA, Duron O, Cordonin C, Gomard Y, Ramasindrazana B, Mavingui P, Goodman SM, Tortosa P. 2016. The bacteriome of bat flies (Nycteribiidae) from the Malagasy region: A community shaped by host ecology, bacterial transmission mode, and host-vector specificity. Applied and Environmental Microbiology. 82:1778–1788. DOI: https://doi.org/10.1128/AEM.03505-15

Supporting Agencies

Association Vahatra, Helmsley Charitable Trust

How to Cite

Ramanantsalama, R. V., Ganzhorn, J. U., Vololona, J., & Goodman, S. M. (2022). Bat flies: source of supplement nutrients for an endemic Malagasy fruit bat. Tropical Zoology, 35(1-2). https://doi.org/10.4081/tz.2022.107