Comparative morphology of tongue surface in Neotropical aerial insectivore bats (Mammalia: Chiroptera)
DOI:
https://doi.org/10.11606/1807-0205/2021.61.86Keywords:
Tongue papillae structure, Comparative anatomy, New World bats, Scanning electron microscopyAbstract
Comparative morphological characters in Neotropical bats are mostly restricted to external and cranio-dentary complexes, and few studies focusing on other morphological complexes have been carried out. In the case of tongue morphology, comparative analyses of the structure have been restricted to the superfamily Noctilionoidea with a wide range of diets, and Molossidae, a strictly aerial insectivore family. In this paper, we studied the morphology of tongue papillae in 10 aerial insectivore Neotropical bat species, representing six families (Emballonuridae, Furipteridae, Thyropteridae, Mormoopidae, Natalidae, and Vespertilionidae), and data from the previous study of Molossidae were compared. We studied tongues in light and scanning electron microscopes following material preparation protocols. We observed two types of sensitive papillae, circumvallate and fungiform, the latter at times presenting a groove surrounding the papillae. Nine mechanic types were observed, one of them, which we called flaky-like, not hitherto described. All Vespertilionoidea families (Vespertilionidae, Natalidae, and Molossidae) presented, as diagnosing characters, fungiform papillae distributed throughout the tongue, as well as anteriorly at the dorsum, and scale-like papillae on the medial lobe directed laterally and anteriorly. Emballonuridae showed the simplest tongue morphology regarding the presence and abundance of some papillae. Families composing the clade Furipteridae + Thyropteridae + Mormoopidae presented small and non-grooved fungiform papillae, and mechanical bifid papillae were absent. In summary, this study has provided additional traits (putative synapomorphies) of the bat tongue to support the clades on the current bat phylogeny.
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Abayomi, T.A.; Ofusori, D.A.; Ayoka, O.A.; Odukoya, S.A.; Omotoso, E.O.; Amegor, F.O.; Ajayi, S.A.; Ojo, G.B. & Oluwayinka, O.P. 2009. A comparative histological study of the tongue of rat (Rattus norvegicus), bat (Eidolon helvum) and Pangolin (Manis tricuspis). International Journal of Morphology, 27(4): 1111-1119.
Abumandour, M. 2014. Morphological comparison of the filiform papillae of New Zealand white rabbits (Oryctolagus cuniculus) as domestic mammals and Egyptian fruit bat (Rousettus aegyptiacus) as wild mammals using scanning electron microscopic specimens. International Journal of Morphology, 32(4): 1407-1417.
Aguirre, L.; Herrel, A. & Van Damme, M.E. 2003. The implication of food hardness for diet in bats. Functional Ecology, 17(2): 201-212. http://doi.org/10.1046/j.1365-2435.2003.00721.x
Emura, S.; Hayakawa, D.; Chen, H.; Shoumura, S.; Atoji, Y. & Agungpriyono, S. 2001. SEM study on the dorsal lingual surface of the lesser dog-faced fruit bat, Cynopterus brachyotis. Okajimas Folia Anatomica Japonica, 78: 123-128. http://doi.org/10.2535/ofaj1936.78.4_123
Ferrarezzi, H. & Gimenez, E.A. 1996. Systematic patterns and the evolution of feeding habitats in Chiroptera (Mammalia: Archonta). Journal of Comparative Biology, 1: 75-94.
Freeman, P.W. 1979. Specialized insectivory: Beetle-eaten and moth-eaten molossid bats. Journal of Mammalogy, 60(3): 467-479.
Freeman, P.W. 1998. Form, function, and evolution in skulls and teeth of bats. In: Kunz, T.H. & Racey, P.A. (Eds.). Bat biology and conservation. Washington DC, Smithsonian Institution Press. p. 140-156.
Freeman, P.W. 2000. Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evolutionary Ecology Research, 2: 317-335.
Gardner, A.L. 1977. Feeding habits. In: Barker, R.J.; Jones-Jr., J.K. & Carter, D.C. (Eds.). Biology of bats of the New World family Phyllostomatidae, Part 2, Endoparasites. Special Publication Museum of Texas Tech University, 13: 1-364, 293-350.
Gimenez, E.A. 1993. Morfologia lingual comparada, filogenia e evolução dos hábitos alimentares na superfamília Phyllostomoidea (Mammalia: Chiroptera). Universidade Estadual Paulista, Botucatu (Master Thesis).
Gimenez, E.A.; Ferrarezzi, H. & Taddei, V.A. 1996. Lingual morphology and cladistics analysis of the New World nectar-feeding bats (Chiroptera: Phyllostomidae). Journal of Comparative Biology, 1: 41-63.
Goloboff, P.A.; Farris, J.S. & Nixon, K.C. 2008. TNT, a free program for phylogenetic analysis. Cladistics, 24: 774-786.
Greenbaum, I.F. & Phillips, C.J. 1974. Comparative anatomy and general histology of the tongues of long-nosed bats (Leptonycteris sanborni and L. nivalis), with reference to infestation of oral mites. Journal of Mammalogy, 55: 489-504.
Gregorin, R. 2003 Comparative morphology of the tongue in free-tailed bats (Chiroptera, Molossidae). Iheringia, Zoologia, 93: 213-221. http://doi.org/10.1590/S0073-47212003000200014
Griffths, T.A. 1982. Systematics of the New World nectar-feeding bats (Mammalia, Phyllostomidae), based on the morphology of the hyoid and lingual regions. American Museum Novitates, 2742: 1-45.
Griffths, T.A. & Criley B.B. 1989. Comparative lingual anatomy of the bats Desmodus rotundus and Lonchophylla robusta (Chiroptera: Phyllostomidae). Journal of Mammalogy, 70: 608-613.
Harper, C.J.; Swartz, S.M. & Brainerd, E.L. 2013. Specialized bat tongue is a hemodynamic nectar mop. Proceedings of the National Academy of Sciences, 110: 8852-8857. http://doi.org/10.1073/pnas.1222726110
Howell, D.J. & Hodgkin, N. 1976. Feeding adaptation in the hairs and tongues of nectar-feeding bats. Journal of Morphology, 148: 329-336.
Jackowiak, H.; Trzcielinska-Lorych, J. & Godynicki, S. 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: 13-21. http://doi.org/10.1679/aohc.72.13
Kobayashi, S. & Shimamura, A. 1982. Comparative anatomical observations of the tongue of the Japonese long-fringered bats, Miniopterus schreibersi fuliginosus. Okajimas Folia Anatomica Japonica, 58: 923-932. http://doi.org/10.2535/ofaj1936.58.4-6_923
Monteiro, L.R. & Nogueira, M.R. 2009. Adaptative radiations, ecological specialization, and the evolutionary integration of complex morphological structures. Evolution, 64: 724-744. http://doi.org/10.1111/j.1558-5646.2009.00857.x
Monteiro, L.R. & Nogueira, M.R. 2011. Evolutionary patterns and processes in the radiation of phyllostomid bats. BMC Evolutionary Biology, 11. http://doi.org/10.1186/1471-2148-11-137
Park, H. & Hall, E.R. 1951. The gross anatomy of tongues and stomachs of eight New World bats. Transactions of the Kansas Academy of Science, 54: 64-72.
Pastor, J.F.; Moro, J.A.; Verona, J.A.G.; Gato, A.; Represa, J.J. & Barbosa, E. 1993. Morphological study by scanning electron microscopy of the lingual papillae in the common European bat (Pipistrellus pipistrellus). Archives of Oral Biology, 38: 597-599. http://doi.org/10.1016/0003-9969(93)90125-6
Rossoni, D.M.; Costa, B.M.A.; Giannini, N.P. & Marroig, G. 2019. A multiple peak adaptative landscape based on feeding strategies and roosting ecology shaped the evolution of cranial covariance structure and morphological differentiation in phyllostomid bats. Evolution, 73: 961-981. http://doi.org/10.1111/evo.13715
Santana, S.E. 2016. Quantifying the effect of gape and morphology on bite force: biomechanical modeling and in vivo measurements in bats. Functional Ecology, 30: 557-565. http://doi.org/10.1111/1365-2435.12522
Simmons, N.B. & Conway, T.M. 2003. Evolution of Ecological Diversity in Bats. In: Kunz, T.H. & Fenton, M.B. (Eds.). Bat Ecology. The University of Chicago Press, Chicago, 493-57.
Teeling, E.C.; Springer, M.S.; Madsen, O.; Bates, P.; O’Brien, S.J. & Murphy, W.J. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science, 307: 580-584. http://doi.org/10.1126/science.1105113
Uieda, W. 1986. Aspectos da morfologia lingual das três espécies de morcegos hematófagos (Chiroptera, Phyllostomidae). Revista Brasileira de Biologia, 46: 581-587.
Wetterer, A.L.; Rockman, M.V. & Simmons, N.B. 2000. Phylogeny of phyllostomid bats (Mammalia: Chiroptera): Data from diverse morphological systems, sex chromosomes, and restriction sites. Bulletin of the American Museum of Natural History, 248: 1-200.
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Conselho Nacional de Desenvolvimento Científico e Tecnológico
Grant numbers 303382/2016-3;402330/2016-1