Bat Tongues and Foraging: Linking Morphology to Hunting Strategies

Abstract

On their dorsal surface, bat tongues show a raised muscular structure called mediodorsal lobe (MDL) or lingual prominence. It exhibits different mechanical papillae across species, which we hypothesized are linked to foraging strategies. We predicted that tall MDLs and prominent papillae pointing frontward would effectively trap prey items caught on the wing by aerial hawkers. We examined 904 high-resolution, close-up images of 239 individual bats from 24 European species, focusing on MDL height and morphology and arrangement of MDL papillae. Aerial hawkers such as Tadarida teniotis, Nyctalus lasiopterus, Miniopterus schreibersii, and pipistrelles displayed prominent forward-pointing papillae and taller MDLs, adaptations suited to high-speed aerial foraging. These traits may be part of a broader “ecomorphological syndrome”, facilitating efficient prey capture in open-space foragers. In contrast, gleaning and trawling species lacked these specializations, exhibiting flatter MDLs and less prominent papillae. Phylogenetic analysis indicated evolutionary convergence in MDL morphology among aerial hawkers, with M. schreibersii showing similarities to vespertilionids despite its phylogenetic distance. This convergence highlights the influence of evolutionary pressures arising from foraging requirements on tongue morphology. Although possessing tall MDLs, rhinolophids are outliers, possibly reflecting their unique perch-hunting strategy or echolocation. If the patterns we found are confirmed for a larger number of species, MDL morphology could predict foraging style across bat species and be included in future descriptions of foraging guilds.

Keywords

Chiroptera / ecomorphology / foraging / guild / tongue

References

[1] Abumandour, M. M., and R. M. El-Bakary. 2013. “Morphological and Scanning Electron Microscopic Studies of the Tongue of the Egyptian Fruit Bat (Rousettus aegyptiacus) and Their Lingual Adaptation for Its Feeding Habits.” Veterinary Research Communications 37: 229–238. https://doi.org/10.1007/s11259-013-9567-9.

[2] Aihartza, J., N. Vallejo, M. Aldasoro, et al. 2023. “Aerospace-foraging Bats Eat Seasonably Across Varying Habitats.” Scientific Reports 13, no. 1: 19576. https://doi.org/10.1038/s41598-023-46939-7.

[3] Aizpurua, O., and A. Alberdi. 2018. “Ecology and Evolutionary Biology of Fishing Bats.” Mammal Review 48, no. 4: 284–297. https://doi.org/10.1111/mam.12136.

[4] Amorim, F., and H. Rebelo. 2011. “Bridging the Gap: The Development of a New Trap Tocapture Bats Roosting in Bridges.” Bat Research News 52, no. 4: 101.

[5] Anderson, M. E., and P. A. Racey. 1991. “Feeding Behaviour of Captive Brown Long-Eared Bats, Plecotus auritus.” Animal Behaviour 42, no. 3: 489–493. https://doi.org/10.1016/S0003-3472(05)80048-X.

[6] Arditti, J., J. Elliott, I. J. Kitching, and L. T. Wasserthal. 2012. “Good Heavens What Insect Can Suck It'–Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta.” Botanical Journal of the Linnean Society 169, no. 3: 403–432. https://doi.org/10.1111/j.1095-8339.2012.01250.x.

[7] Arlettaz, R. 1996. “Feeding Behaviour and Foraging Strategy of Free-Living Mouse-Eared Bats, Myotis myotis and Myotis blythii.” Animal Behaviour 51, no. 1: 1–11. https://doi.org/10.1006/anbe.1996.0001.

[8] Arlettaz, R., G. Jones, and P. A. Racey. 2001. “Effect of Acoustic Clutter on Prey Detection by Bats.” Nature 414: 742–745. https://doi.org/10.1038/414742a.

[9] Arlettaz, R., N. Perrin, and J. Hausser. 1997. “Trophic Resource Partitioning and Competition Between the Two Sibling Bat Species Myotis myotis and Myotis blythii.” Journal of Animal Ecology 66, no. 6: 897–911. https://doi.org/10.2307/6005.

[10] Bogdanowicz, W., M. B. Fenton, and K. Daleszczyk. 1999. “The Relationships Between Echolocation Calls, Morphology and Diet in Insectivorous Bats.” Journal of Zoology 247, no. 3: 381–393. https://doi.org/10.1111/j.1469-7998.1999.tb01001.x.

[11] Budinski, I., and A. López-Baucells. 2023. “Myotis mystacinus Species Complex (M. mystacinus, M. brandtii, M. alcathoe, M. davidii).” In Chiroptera. Handbook of the Mammals of Europe, edited by D. Russo. Springer. https://doi.org/10.1007/978-3-030-44029-9_53.

[12] Cooper, W. E., Jr. 1994. “Multiple Functions of Extraoral Lingual Behaviour in Iguanian Lizards: Prey Capture, Grooming and Swallowing, but Not Prey Detection.” Animal Behaviour 47, no. 4: 765–775. https://doi.org/10.1006/anbe.1994.1109.

[13] Datzmann, T., O. von Helversen, and F. Mayer. 2010. “Evolution of Nectarivory in Phyllostomid Bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia).” BMC Evolutionary Biology 10: 165. https://doi.org/10.1186/1471-2148-10-165.

[14] Denzinger, A., and H. U. Schnitzler. 2013. “Bat Guilds, a Concept to Classify the Highly Diverse Foraging and Echolocation Behaviors of Microchiropteran Bats.” Frontiers in Physiology 4: 164. https://doi.org/10.3389/fphys.2013.00164.

[15] Dietz, C., and A. Kiefer. 2016. Bats of Britain and Europe. Bloomsbury publishing.

[16] Dietz, M., and J. B. Pir. 2021. “Geoffroy's Bat Myotis emarginatus (Geoffroy, 1806).” In Handbook of the Mammals of Europe, edited by K. Hackländer and F. E. Zachos. Springer. https://doi.org/10.1007/978-3-319-65038-8_56-1.

[17] El-Mansi, A. A., M. A. Al-Kahtani, and M. M. Abumandour. 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. https://doi.org/10.1016/j.jcz.2019.05.005.

[18] Faurby, S., and J. C. Svenning. 2015. “A Species-Level Phylogeny of all Extant and Late Quaternary Extinct Mammals Using a Novel Heuristic-Hierarchical Bayesian Approach.” Molecular Phylogenetics and Evolution 84: 14–26. https://doi.org/10.1016/j.ympev.2014.11.001.

[19] Goerlitz, H. R., H. M. ter Hofstede, M. R. Zeale, G. Jones, and M. W. Holderied. 2010. “An Aerial-Hawking Bat Uses Stealth Echolocation to Counter Moth Hearing.” Current Biology 20, no. 17: 1568–1572. https://doi.org/10.1016/j.cub.2010.07.046.

[20] Gregorin, R. 2003. “Comparative Morphology of the Tongue in Free-Tailed Bats (Chiroptera, Molossidae).” Iheringia. Série Zoologia 93: 213–221. https://doi.org/10.1590/S0073-47212003000200014.

[21] Gregorin, R., and P. A. Zanatta. 2021. “Comparative Morphology of Tongue Surface in Neotropical Aerial Insectivore Bats (Mammalia: Chiroptera).” Papéis Avulsos De Zoologia 61: e20216186. https://doi.org/10.11606/1807-0205/2021.61.86.

[22] Gual-Suárez, F., and R. A. Medellin. 2021. “We Eat Meat: A Review of Carnivory in Bats.” Mammal Review 51, no. 4: 540–558. https://doi.org/10.1111/mam.12254.

[23] Hansen, T. F., and S. H. Orzack. 2005. “Assessing Current Adaptation and Phylogenetic Inertia as Explanations of Trait Evolution: The Need for Controlled Comparisons.” Evolution; International Journal of Organic Evolution 59, no. 10: 2063–2072.

[24] Ibáñez, C., A. G. Popa-Lisseanu, D. Pastor-Beviá, J. L. García-Mudarra, and J. Juste. 2016. “Concealed by Darkness: Interactions Between Predatory Bats and Nocturnally Migrating Songbirds Illuminated by DNA Sequencing.” Molecular Ecology 25, no. 20: 5254–5263. https://doi.org/10.1111/mec.13831.

[25] Iwasaki, S. I. 2002. “Evolution of the Structure and Function of the Vertebrate Tongue.” Journal of Anatomy 201, no. 1: 1–13. https://doi.org/10.1046/j.1469-7580.2002.00073.x.

[26] Jackowiak, H., J. Trzcielinska-Lorych, and S. Godynicki. 2009. “The Microstructure of Lingual Papillae in the Egyptian Fruit Bat (Rousettus aegyptiacus) as Observed by Light Microscopy and Scanning Electron Microscopy.” Archives of Histology and Cytology 72, no. 1: 13–21. https://doi.org/10.1679/aohc.72.13.

[27] Kalko, E. K., and H. U. Schnitzler. 1989. “The Echolocation and Hunting Behavior of Daubenton's Bat, Myotis daubentoni.” Behavioral Ecology and Sociobiology 24: 225–238. https://doi.org/10.1007/BF00295202.

[28] Kingston, T. 2013. “Response of Bat Diversity to Forest Disturbance in Southeast Asia: Insights from Long-Term Research in Malaysia.” In Bat Evolution, Ecology, and Conservation, edited by R. Adams and S. Pedersen, 169–185. Springer.

[29] Kinnamon, S. C., and T. A. Cummings. 1992. “Chemosensory Transduction Mechanisms in Taste.” Annual Review of Physiology 54, no. 1: 715–731. https://doi.org/10.1146/annurev.ph.54.030192.003435.

[30] Lewanzik, D., J. M. Ratcliffe, E. A. Etzler, H. R. Goerlitz, and L. Jakobsen. 2023. “Stealth Echolocation in Aerial Hawking Bats Reflects a Substrate Gleaning Ancestry.” Current Biology 33, no. 23: 5208–5214. https://doi.org/10.1016/j.cub.2023.10.014.

[31] Luo, B., L. Leiser-Miller, S. E. Santana, et al. 2019. “Echolocation Call Divergence in Bats: A Comparative Analysis.” Behavioral Ecology and Sociobiology 73, no. 11: 154. https://doi.org/10.1007/s00265-019-2766-9.

[32] Martinoli, A., M. V. Mazzamuto, and M. Spada. 2023. “Serotine Eptesicus serotinus (Schreber, 1774).” In Chiroptera. Handbook of the Mammals of Europe, edited by D. Russo. Springer. https://doi.org/10.1007/978-3-030-44029-9_44.

[33] Massoud, D., and M. M. Abumandour. 2020. “Anatomical Features of the Tongue of Two Chiropterans Endemic in the Egyptian Fauna; the Egyptian Fruit Bat (Rousettus aegyptiacus) and Insectivorous Bat (Pipistrellus kuhlii).” Acta Histochemica 122, no. 2: 151503. https://doi.org/10.1016/j.acthis.2020.151503.

[34] Masuko, T. S., S. N. Boaro, B. König-Junior, R. H. Cabral, and O. Paulo. 2007. “Comparative Scanning Electron Microscopic Study of the Lingual Papillae in Three Species of Bats (Carollia perspicillata, Glossophaga soricina and Desmodus rotundus).” Microscopy and Microanalysis 13, no. S02: 280–281. https://doi.org/10.1017/S1431927607078890.

[35] Miller-Butterworth, C. M., W. J. Murphy, S. J. O'Brien, D. S. Jacobs, M. S. Springer, and E. C. Teeling. 2007. “A Family Matter: Conclusive Resolution of the Taxonomic Position of the Long-Fingered Bats, Miniopterus.” Molecular Biology and Evolution 24, no. 7: 1553–1561. https://doi.org/10.1093/molbev/msm076.

[36] Mooring, M. S., D. T. Blumstein, and C. J. Stoner. 2004. “The Evolution of Parasite-Defence Grooming in Ungulates.” Biological Journal of the Linnean Society 81, no. 1: 17–37. https://doi.org/10.1111/j.1095-8312.2004.00273.x.

[37] Muchhala, N. 2006. “Nectar Bat Stows Huge Tongue in Its Rib Cage.” Nature 444, no. 7120: 701–702. https://doi.org/10.1038/444701a.

[38] Noel, A. C., and D. L. Hu. 2018. “The Tongue as a Gripper.” Journal of Experimental Biology 221, no. 7: jeb176289. https://doi.org/10.1242/jeb.176289.

[39] Norberg, U. M. 1986. “Evolutionary Convergence in Foraging Niche and Flight Morphology in Insectivorous Aerial-Hawking Birds and Bats.” Ornis Scandinavica 17, no. 3: 253–260. https://doi.org/10.2307/3676835.

[40] Norberg, U. M., and J. M. V Rayner. 1987. “Ecological Morphology and Flight in Bats (Mammalia; Chiroptera): Wing Adaptations, Flight Performance, Foraging Strategy and Echolocation.” Philosophical Transactions of the Royal Society 316, no. 1179: 335–427. https://doi.org/10.1098/rstb.1987.0030.

[41] O'Mara, M. T., F. Amorim, M. Scacco, et al. 2021. “Bats Use Topography and Nocturnal Updrafts to Fly High and Fast.” Current Biology 31, no. 6: 1311–1316. https://doi.org/10.1016/j.cub.2020.12.042.

[42] Orr, T. J., J. Ortega, R. A. Medellín, C. D. Sánchez, and K. A. Hammond. 2016. “Diet Choice in Frugivorous Bats: Gourmets or Operational Pragmatists?” Journal of Mammalogy 97, no. 6: 1578–1588. https://doi.org/10.1093/jmammal/gyw122.

[43] Park, J. W., and J. H. Lee. 2009. “Comparative Morphology of the Tongue of Miniopterus schreibersi fuliginosus and Pipistrellus savii.” Applied Microscopy 39, no. 3: 267–276.

[44] Pastor, J. F., J. A. Moro, J. A. G. Verona, A. Gato, J. J. Represa, and E. Barbosa. 1993. “Morphological Study by Scanning Electron Microscopy of the Lingual Papillae in the Common European Bat (Pipistrellus pipistrellus).” Archives of Oral Biology 38, no. 7: 597–599. https://doi.org/10.1016/0003-9969(93)90125-6.

[45] Riskin, D. K., and G. G. Carter. 2023. “The Evolution of Sanguivory in Vampire Bats: Origins and Convergences.” Canadian Journal of Zoology 101, no. 4: 207–221. https://doi.org/10.1139/cjz-2022-0115.

[46] Russo, D., L. Ancillotto, A. C. Hughes, A. Galimberti, and E. Mori. 2017. “Collection of Voucher Specimens for Bat Research: Conservation, Ethical Implications, Reduction, and Alternatives.” Mammal Review 47, no. 4: 237–246. https://doi.org/10.1111/mam.12095.

[47] Saragih, G. R., G. Gunawan, Y. Umardani, S. Karnati, D. L. Kusindarta, and H. Wihadmadyatami. 2020. “Morphological and Scanning Electron Microscopic Study of the Lingual Papillae in the Javan Pipistrelle (Pipistrellus javanicus).” Anatomia, Histologia, Embryologia 49, no. 6: 718–727. https://doi.org/10.1111/ahe.12566.

[48] Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. 2012. “NIH Image to ImageJ: 25 Years of Image Analysis.” Nature Methods 9, no. 7: 671–675. https://doi.org/10.1038/nmeth.2089.

[49] Sharma, R. S. K., M. K. Vidyadaran, I. Zulkifli, et al. 1999. “Ecomorphological Implications of the Microstructures on the Tongue of the Fawn Roundleaf Bat, Hipposideros cervinus (Chiroptera: Hipposideridae).” Australian Journal of Zoology 47, no. 4: 405–409. https://doi.org/10.1071/ZO98051.

[50] Simmons, N. B. 2005. “Order Chiroptera.” In Mammal Species of the World: A Taxonomic and Geographic Reference, edited by D. E. Wilson and D. M. Reeder, 312–529. vol. 1. The Johns Hopkins University Press.

[51] Simmons, N. B., and A. L. Cirranello. 2025. "Bat Species of the World: A Taxonomic and Geographic Database." Version 1.7. Accessed on March 29, 2025. https://batnames.org.

[52] Stoffberg, S., D. S. Jacobs, I. J. Mackie, and C. A. Matthee. 2010. “Molecular Phylogenetics and Historical Biogeography of Rhinolophus Bats.” Molecular Phylogenetics and Evolution 54, no. 1: 1–9. https://doi.org/10.1016/j.ympev.2009.09.021.

[53] Teeling, E. C., O. Madsen, R. A. Van Den Bussche, W. W. de Jong, M. J. Stanhope, and M. S. Springer. 2002. “Microbat Paraphyly and the Convergent Evolution of a Key Innovation in Old World Rhinolophoid Microbats.” Proceedings of the National Academy of Sciences 99, no. 3: 1431–1436. https://doi.org/10.1073/pnas.022477199.

[54] Trzcielińska-Lorych, J., H. Jackowiak, K. Skieresz-Szewczyk, and S. Godynicki. 2009. “Morphology and Morphometry of Lingual Papillae in Adult and Newborn Egyptian Fruit Bats (Rousettus aegyptiacus).” Anatomia, Histologia, Embryologia 38, no. 5: 370–376. https://doi.org/10.1111/j.1439-0264.2009.00956.x.

[55] Tschapka, M., T. P. Gonzalez-Terrazas, and M. Knörnschild. 2015. “Nectar Uptake in Bats Using a Pumping-Tongue Mechanism.” Science Advances 1, no. 8: e1500525. https://doi.org/10.1126/sciadv.1500525.

[56] Voigt, C. C., B. M. Schuller, S. Greif, and B. M. Siemers. 2010. “Perch-Hunting in Insectivorous Rhinolophus Bats Is Related to the High Energy Costs of Manoeuvring in Flight.” Journal of Comparative Physiology B 180: 1079–1088. https://doi.org/10.1007/s00360-010-0466-x.

[57] Zou, W., H. Liang, P. Wu, et al. 2022. “Correlated Evolution of Wing Morphology and Echolocation Calls in Bats.” Frontiers in Ecology and Evolution 10. https://doi.org/10.3389/fevo.2022.1031548.

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