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Dietary and body-mass reconstruction of the Miocene neotropical bat Notonycteris magdalenensis (Phyllostomidae) from La Venta, Colombia

Published online by Cambridge University Press:  12 July 2021

Camilo López-Aguirre Open the ORCID record for Camilo López-Aguirre [Opens in a new window] ,
Nicholas J. Czaplewski ,
Andrés Link ,
Masanaru Takai  and
Suzanne J. Hand
Camilo López-Aguirre*
Affiliation:
Earth and Sustainability Science Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney 2052, Australia. E-mail: s.hand@unsw.edu.au.
Nicholas J. Czaplewski
Affiliation:
Section of Vertebrate Paleontology, Oklahoma Museum of Natural History, Norman, Oklahoma 73072, U.S.A. E-mail: nczaplewski@ou.edu
Andrés Link
Affiliation:
Departamento de Ciencias Biológicas, Universidad de los Andes, 111711 Bogotá DC, Colombia. E-mail: a.link74@uniandes.edu.co
Masanaru Takai
Affiliation:
Primate Research Institute, Kyoto University, 606-8585 Inuyama, Japan. E-mail: takai.masanaru.2s@kyoto-u.ac.jp
Suzanne J. Hand
Affiliation:
Earth and Sustainability Science Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney 2052, Australia. E-mail: s.hand@unsw.edu.au.
*
*Corresponding author.
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Abstract

With 14 species recorded, the Miocene La Venta bat fauna is the most diverse bat paleocommunity in South America. It includes the oldest plant-visiting bat in the New World and some of the earliest representatives of the extant families Phyllostomidae, Thyropteridae, and Noctilionidae. La Venta's Notonycteris magdalenensis is an extinct member of the subfamily Phyllostominae, a group of modern Neotropical animalivorous bats, and is commonly included in studies of the evolution of Neotropical bats, but aspects of its biology remain unclear. In this study, we used multivariate dental topography analysis (DTA) to reconstruct the diet of N. magdalenensis by quantitatively comparing measures of molar complexity with those of 25 modern noctilionoid species representing all major dietary habits in bats. We found clear differences in molar complexity between dietary guilds, indicating that DTA is potentially an informative tool to study bat ecomorphology. Our results suggest N. magdalenensis was probably an omnivore or insectivore, rather than a carnivore like its modern relatives Chrotopterus auritus and Vampyrum spectrum. Also, we reconstructed the body mass of N. magdalenensis to be ~95 g, larger than most insectivorous bats, but smaller than the largest carnivorous bat (V. spectrum). Our results confirm that N. magdalenensis was not a specialized carnivore. It remains to be demonstrated that the specialized carnivory ecological niche was occupied by the same lineage of phyllostomines from at least the middle Miocene. Combining our diet and body-mass reconstructions, we suggest that N. magdalenensis exhibits morphological pre-adaptations crucial for the evolution of specialized carnivory.

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Paleobiology , Volume 48 , Issue 1 , February 2022 , pp. 137 - 153
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Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society

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Footnotes

†

Present address: Department of Anthropology, University of Toronto Scarborough, Toronto M1C 1A4, Canada. E-mail: c.lopezaguirre@utoronto.ca

References

Literature Cited

Adams, D. C. 2014. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Systematic Biology 63:685–697.CrossRefGoogle ScholarPubMed
Aguirre, L. F., Herrel, A., van Damme, R., and Matthysen, E.. 2002. Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proceedings of the Royal Society of London B 269:1271–1278.CrossRefGoogle Scholar
Aguirre, L. F., Herrel, A., Van Damme, R., and Matthysen, E.. 2003. The implications of food hardness for diet in bats. Functional Ecology 17:201–212.CrossRefGoogle Scholar
Allen, K. L., Cooke, S. B., Gonzales, L. A., and Kay, R. F.. 2015. Dietary inference from upper and lower molar morphology in platyrrhine primates. PLoS ONE 10:e0118732.CrossRefGoogle ScholarPubMed
Amador, L. I., Moyers Arévalo, R. L., Almeida, F. C., Catalano, S. A., and Giannini, N. P.. 2016. Bat systematics in the light of unconstrained analyses of a comprehensive molecular supermatrix. Journal of Mammalian Evolution 25:37–70CrossRefGoogle Scholar
Amador, L. I., Simmons, N. B., and Giannini, N. P.. 2019. Aerodynamic reconstruction of the primitive fossil bat Onychonycteris finneyi (Mammalia: Chiroptera). Biology Letters 15:20180857.CrossRefGoogle Scholar
Arbour, J. H., Curtis, A. A., and Santana, S. E.. 2019. Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats. Nature Commununications 10:2036.CrossRefGoogle ScholarPubMed
Arévalo, R. L. M. 2020. The evolution of body size in noctilionoid bats. Pp. 123–148 in Fleming, T. H., Dávalos, L. M., and Mello, Marco A. R., eds. Phyllostomid bats: a unique mammalian radiation. University of Chicago Press, Chicago.Google Scholar
Baker, R. J., Bininda-Emonds, O. R. P., Mantilla-Meluk, H., Porter, C. A., and Van Den Bussche, R. A.. 2012. Molecular time scale of diversification of feeding strategy and morphology in New World leaf-nosed bats (Phyllostomidae): a phylogenetic perspective. Pp. 385–409 in Gunnell, G. F. and Simmons, N. B., eds. Evolutionary history of bats: fossils, molecules and morphology. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Baker, R. J., Solari, S., Cirranello, A., and Simmons, N.. 2016. higher level classification of phyllostomid bats with a summary of DNA synapomorphies. Acta Chiropterologica 18:1–38CrossRefGoogle Scholar
Berkovitz, B., and Shellis, P.. 2018. Chiroptera. Pp. 187–211 in Berkovitz, B. and Shellis, P., eds. The teeth of mammalian vertebrates. Academic Press, Cambridge, Mass.CrossRefGoogle Scholar
Berthaume, M. A., Winchester, J., and Kupczik, K.. 2019a. Ambient occlusion and PCV (portion de ciel visible): a new dental topographic metric and proxy of morphological wear resistance. PLoS ONE 14:e0215436.CrossRefGoogle Scholar
Berthaume, M. A., Winchester, J., and Kupczik, K.. 2019b. Effects of cropping, smoothing, triangle count, and mesh resolution on 6 dental topographic metrics. PLoS ONE 14:e0216229.CrossRefGoogle Scholar
Berthaume, M. A., Lazzari, V., and Guy, F.. 2020. The landscape of tooth shape: over 20 years of dental topography in primates. Evolutionary Anthropology 29:245–262.CrossRefGoogle ScholarPubMed
Bolzan, D. P., Pessôa, L. M., Peracchi, A. L., and Strauss, R. E.. 2015. Allometric patterns and evolution in Neotropical nectar-feeding bats (Chiroptera, Phyllostomidae). Acta Chiropterologica 17:59–73.CrossRefGoogle Scholar
Boyer, D. 2008. Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. Journal of Human Evolution 55 6:1118–1137.CrossRefGoogle Scholar
Brokaw, A. F., and Smotherman, M.. 2020. Role of ecology in shaping external nasal morphology in bats and implications for olfactory tracking. PLoS One 15:e0226689.CrossRefGoogle ScholarPubMed
Brown, E. E., Cashmore, D. D., Simmons, N. B., and Butler, R. J.. 2019. Quantifying the completeness of the bat fossil record. Palaeontology 62:757–776.CrossRefGoogle Scholar
Bunn, J. M., and Ungar, P. S.. 2009. Dental topography and diets of four Old World monkey species. American Journal of Primatology 71:466–477.CrossRefGoogle ScholarPubMed
Bunn, J. M., Boyer, D. M., Lipman, Y., St Clair, E. M., Jernvall, J., and Daubechies, I.. 2011. Comparing Dirichlet normal surface energy of tooth crowns, a new technique of molar shape quantification for dietary inference, with previous methods in isolation and in combination. American Journal of Physical Anthropology 145:247–261.CrossRefGoogle ScholarPubMed
Cooke, S. B. 2011. Paleodiet of extinct platyrrhines with emphasis on the Caribbean forms: three-dimensional geometric morphometrics of mandibular second molars. Anatomical Record 294:2073–2091.CrossRefGoogle ScholarPubMed
Croft, D. A. 2001. Cenozoic environmental change in South America as indicated by mammalian body size distributions (cenograms). Diversity and Distributions 7:271–287.CrossRefGoogle Scholar
Croft, D. A. 2016. Horned armadillos and rafting monkeys. Indiana University Press, Bloomington.Google Scholar
Curtis, A. A., and Santana, S. E.. 2018. Jaw-dropping: functional variation in the digastric muscle in bats. Anatomical Record 301:279–290.CrossRefGoogle ScholarPubMed
Czaplewski, N. J. 1997. Chiroptera. Pp. 410–431 in Kay, R. F., Madden, R. H., Cifelli, R. L., and Flynn, J. J., eds. Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, D.C.Google Scholar
Czaplewski, N. J., Takai, M., Naeher, T. M., Shigehara, Nobuo, Setoguchi, T., and Shigehara, N.. 2003. Additional bats from the middle Miocene of La Venta fauna of Colombia. Revista de la Academia Colombiana de Ciencias 27:263–282.Google Scholar
Datzmann, T., von Helversen, O., and Mayer, F.. 2010. Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Evolutionary Biology 10:165.CrossRefGoogle Scholar
Dávalos, L. M., Velazco, P. M., Warsi, O. M., Smits, P. D., and Simmons, N. B.. 2014. Integrating incomplete fossils by isolating conflicting signal in saturated and non-independent morphological characters. Systematic Biology 63:582–600.CrossRefGoogle ScholarPubMed
Davies, K. T. J., Yohe, L. R., Almonte, J., Sánchez, M. K. R., Rengifo, E. M., Dumont, E. R., Sears, K. E., Dávalos, L. M., and Rossiter, S. J.. 2020. Foraging shifts and visual preadaptation in ecologically diverse bats. Molecular Ecology 29:1839–1859.CrossRefGoogle ScholarPubMed
Denzinger, A., and Schnitzler, H. U.. 2013. Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Frontiers in Physiology 4:164.CrossRefGoogle ScholarPubMed
Dumont, E. R., Davalos, L. M., Goldberg, A., Santana, S. E., Rex, K., and Voigt, C. C.. 2012. Morphological innovation, diversification and invasion of a new adaptive zone. Proceedings of the Royal Society of London B 279:1797–1805.Google ScholarPubMed
Eiting, T. P., and Gunnell, G. F.. 2009. Global completeness of the bat fossil record. Journal of Mammalian Evolution 16:151–173.CrossRefGoogle Scholar
Evans, A. R., Wilson, G. P., Fortelius, M., and Jernvall, J.. 2007. High-level similarity of dentitions in carnivorans and rodents. Nature 445:78–81.CrossRefGoogle ScholarPubMed
Fernando, G., Roberto, M., Priscila, C., and Erich, F.. 2007. Feeding habits of Noctilio albiventris (Noctilionidae) bats in the Pantanal, Brazil. Acta Chiropterologica 9:535–538.Google Scholar
Fleming, T. H. 1986. Opportunism versus specialization: the evolution of feeding strategies in frugivorous bats. Pp. 105–118 in Estrada, A. and Fleming, T. H., eds. Frugivores and seed dispersal. Springer, Dordrecht, Netherlands.CrossRefGoogle Scholar
Fleming, T. H., Dávalos, L. M., and Mello, M. A. R.. 2020. Phyllostomid bats: a unique mammalian radiation. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Freeman, P. W. 1981. Correspondence of food habits and morphology in insectivorous bats. Journal of Mammalogy 62:166–173.CrossRefGoogle Scholar
Freeman, P. W. 1988. Frugivorous and animalivorous bats (Microchiroptera): dental and cranial adaptations. Biological Journal of the Linnean Society 33:249–272.CrossRefGoogle Scholar
Freeman, P. W. 1995. Nectarivorous feeding mechanisms in bats. Biological Journal of the Linnean Society 56:439–463.CrossRefGoogle Scholar
Freeman, P. W. 1998. Form, function, and evolution in skulls and teeth of bats. Pp. 140–156 in Kunz, T. H. and Racey, P. A., eds. Bat biology and conservation. Smithsonian Institution Press, Washington, D.C.Google Scholar
Freeman, P. W. 2000. Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evolutionary Ecology Research 2:317–335.Google Scholar
Gaudioso, P. J., Martínez, J. J., Barquez, R. M., and Díaz, M. M.. 2020. Evolution of scapula shape in several families of bats (Chiroptera, Mammalia). Journal of Zoological Systematics and Evolutionary Research 58:1374–1394.CrossRefGoogle Scholar
Giannini, N. P., Gunnell, G. F., Habersetzer, J., and Simmons, N. B.. 2012. Early evolution of body size in bats. Pp. 530–555 in Gunnell, G. F. and Simmons, N. B., eds. Evolutionary history of bats: fossils, molecules and morphology. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Giannini, N. P., Amador, L. I., and Moyers-Arévalo, R. L.. 2020. The evolution of body size in noctilionoid bats. Pp. 123–148 in Fleming, T. H., Dávalos, L. M., and Mello, M. A. R., eds. Phyllostomid bats: a unique mammalian radiation. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Guerrero, J. 1997. Stratigraphy, Sedimentary Environments, and the Miocene Uplift of the Colombian Andes. Pp. 15–43 in Kay, R., Madden, R., Cifelli, R. L., and Flynn, J., eds. Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, D.C.Google Scholar
Gunnell, G. F., and Simmons, N. B.. 2005. Fossil evidence and the origin of bats. Journal of Mammalian Evolution 12:209–246.CrossRefGoogle Scholar
Gunnell, G. F., Worsham, S. R., Seiffert, E. R., and Simons, E. L.. 2009. Vampyravus orientalis Schlosser (Chiroptera) from the Early Oligocene (Rupelian), Fayum, Egypt—body mass, humeral morphology and affinities. Acta Chiropterologica 11:271–278.Google Scholar
Hand, S., Sigé, B., Archer, M., and Black, K.. 2016. An evening bat (Chiroptera: Vespertilionidae) from the late Early Eocene of France, with comments on the antiquity of modern bats. Palaeovertebrata 40:e2.CrossRefGoogle Scholar
Hand, S. J. 1985. New Miocene megadermatids (Chiroptera: Megadermatidae) from Australia with comments on megadermatid phylogenetics. Australian Mammalogy 8:5–43.Google Scholar
Hand, S. J. 1996. New Miocene and Pliocene megadermatids (Mammalia, Microchiroptera) from Australia, with comments on broader aspects of megadermatid evolution. Geobios 29:365–377.CrossRefGoogle Scholar
Hand, S. J. 1998. Xenorhinos, a new genus of Old World leaf-nosed bats (Microchiroptera: Hipposideridae) from the Australian Miocene. Journal of Vertebrate Paleontology 18:430–439.CrossRefGoogle Scholar
Hand, S. J., and Archer, M.. 2005. A new hipposiderid genus (Microchiroptera) from an Early Miocene bat community in Australia. Palaeontology 48:371–383.CrossRefGoogle Scholar
Hand, S. J., and Sigé, B.. 2018. A new archaic bat (Chiroptera: Archaeonycteridae) from an Early Eocene forest in the Paris Basin. Historical Biology 30:227–236.CrossRefGoogle Scholar
Hand, S. J., Lee, D. E., Worthy, T. H., Archer, M., Worthy, J. P., Tennyson, A. J. D., Salisbury, S. W., Scofield, R. P., Mildenhall, D. C., Kennedy, E. M., and Linqvist, J. K.. 2015a. Miocene fossils reveal ancient roots for New Zealand's endemic Mystacina (Chiroptera) and its rainforest habitat. PLoS ONE 10:e0128871.CrossRefGoogle Scholar
Hand, S. J., Sigé, B., Archer, M., Gunnell, G. F., and Simmons, N. B.. 2015b. A new Early Eocene (Ypresian) bat from Pourcy, Paris Basin, France, with comments on patterns of diversity in the earliest chiropterans. Journal of Mammalian Evolution 22:343–354.CrossRefGoogle Scholar
Hand, S. J., Beck, R. M. D., Archer, M., Simmons, N. B., Gunnell, G. F., Scofield, R. P., Tennyson, A. J. D., De Pietri, V. L., Salisbury, S. W., and Worthy, T. H.. 2018. A new, large-bodied omnivorous bat (Noctilionoidea: Mystacinidae) reveals lost morphological and ecological diversity since the Miocene in New Zealand. Scientific Reports 8:235.CrossRefGoogle ScholarPubMed
Hedrick, B. P., Mutumi, G. L., Munteanu, V. D., Sadier, A., Davies, K. T. J., Rossiter, S. J., Sears, K. E., Dávalos, L. M., and Dumont, E.. 2020. Morphological diversification under high integration in a hyper diverse mammal clade. Journal of Mammalian Evolution 27:563–575.CrossRefGoogle Scholar
Hoffmann, F. G., Hoofer, S. R., and Baker, R. J.. 2008. Molecular dating of the diversification of Phyllostominae bats based on nuclear and mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 49:653–658.CrossRefGoogle ScholarPubMed
Hoorn, C. 1994. An environmental reconstruction of the palaeo–Amazon River system (Middle–Late Miocene, NW Amazonia). Palaeogeography, Palaeoclimatology, Palaeoecology 112:187–238.CrossRefGoogle Scholar
Hoorn, C., Guerrero, J., Sarmiento, G. A., and Lorente, M. A.. 1995. Andean tectonics as a cause for changing drainage patterns in Miocene northern South America. Geology 23:237–240.2.3.CO;2>CrossRefGoogle Scholar
Jacobs, D. S., Bastian, A., and Bam, L.. 2014. The influence of feeding on the evolution of sensory signals: a comparative test of an evolutionary trade-off between masticatory and sensory functions of skulls in southern African horseshoe bats (Rhinolophidae). Journal of Evolutionary Biology 27:2829–2840.CrossRefGoogle Scholar
Jones, M. F., Coster, P. M. C., Licht, A., Métais, G., Ocakoğlu, F., Taylor, M. H., and Beard, K. C.. 2019. A stem bat (Chiroptera: Palaeochiropterygidae) from the late middle Eocene of northern Anatolia: implications for the dispersal and palaeobiology of early bats. Palaeobiodiversity and Palaeoenvironments 99:261–269.CrossRefGoogle Scholar
Kalko, E. K. V., Schnitzler, H.-U., Kaipf, I., and Grinnell, A. D.. 1998. Echolocation and foraging behavior of the lesser bulldog bat, Noctilio albiventris : preadaptations for piscivory? Behavioral Ecology and Sociobiology 42:305–319.CrossRefGoogle Scholar
Kay, R. F., and Madden, R. H.. 1997. Mammals and rainfall: paleoecology of the middle Miocene at La Venta (Colombia, South America). Journal of Human Evolution 32:161–199.CrossRefGoogle Scholar
Lazzari, V., Charles, C., Tafforeau, P., Vianey-Liaud, M., Aguilar, J.-P., Jaeger, J.-J., Michaux, J., and Viriot, L.. 2008. Mosaic convergence of rodent dentitions. PLoS ONE 3:e3607.CrossRefGoogle ScholarPubMed
Ledogar, J. A., Winchester, J. M., St. Clair, E. M., and Boyer, D. M.. 2013. Diet and dental topography in pitheciine seed predators. American Journal of Physical Anthropology 150:107–121.CrossRefGoogle ScholarPubMed
Ledogar, J. A., Luk, T. H. Y., Perry, J. M. G., Neaux, D., and Wroe, S.. 2018. Biting mechanics and niche separation in a specialized clade of primate seed predators. PLoS ONE 13:e0190689.CrossRefGoogle Scholar
Leiser-Miller, L. B., and Santana, S. E.. 2020. Morphological diversity in the sensory system of phyllostomid bats: implications for acoustic and dietary ecology. Functional Ecology 34:1416–1427.CrossRefGoogle Scholar
López-Aguirre, C., Hand, S. J., Koyabu, D., Tu, V. T., Wilson, L. A. 2021. Phylogeny and foraging behaviour shape modular morphological variation in bat humeri. Journal of Anatomy 238:1312–1329.CrossRefGoogle ScholarPubMed
López-Torres, S., Selig, K. R., Prufrock, K. A., Lin, D., and Silcox, M. T.. 2018. Dental topographic analysis of paromomyid (Plesiadapiformes, Primates) cheek teeth: more than 15 million years of changing surfaces and shifting ecologies. Historical Biology 30:76–88.CrossRefGoogle Scholar
Louzada, N. S. V., Nogueira, M. R., and Pessôa, L. M.. 2019. Comparative morphology and scaling of the femur in yangochiropteran bats. Journal of Anatomy 235:124–150.Google ScholarPubMed
Madden, R., Guerrero, J., Kay, R., Flynn, J., Iii, C., and Walton, A.. 1997. The Laventan Stage and Age: new chronostratigraphic and geochronologic units for the Miocene of South America. Pp. 499–519 in Kay, R., Madden, R., Cifelli, R. L., and Flynn, J. J., eds. Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian Instituion Press, Washington, D.C.Google Scholar
Melstrom, K. M., and Irmis, R. B.. 2019. Repeated evolution of herbivorous crocodyliforms during the age of dinosaurs. Current Biology 29:2389–2395.CrossRefGoogle ScholarPubMed
Molinari, J., Bustos, X. E., Burneo, S. F., Camacho, M. A., Moreno, S. A., and Fermín, G.. 2017. A new polytypic species of yellow-shouldered bats, genus Sturnira (Mammalia: Chiroptera: Phyllostomidae), from the Andean and coastal mountain systems of Venezuela and Colombia. Zootaxa 4243:22.CrossRefGoogle Scholar
Monteiro, L. R., and Nogueira, M. R.. 2011. Evolutionary patterns and processes in the radiation of phyllostomid bats. BMC Evolutionary Biology 11:137.CrossRefGoogle ScholarPubMed
Montes, C., Silva, C. A., Bayona, G. A., Villamil, R., Stiles, E., Rodriguez-Corcho, A. F., Beltran-Triviño, A., Lamus, F., Muñoz-Granados, M. D., Perez-Angel, L. C., Hoyos, N., Gomez, S., Galeano, J. J., Romero, E., Baquero, M., Cardenas-Rozo, A. L., and von Quadt, A. 2021. A Middle to Late Miocene trans-Andean portal: geologic record in the Tatacoa Desert. Frontiers in Earth Science 8:587022CrossRefGoogle Scholar
Morales, A. E., Ruedi, M., Field, K., and Carstens, B. C.. 2019. Diversification rates have no effect on the convergent evolution of foraging strategies in the most speciose genus of bats, Myotis. Evolution 73:2263–2280.CrossRefGoogle ScholarPubMed
Moyers Arévalo, R. L., Amador, L. I., Almeida, F. C., and Giannini, N. P.. 2020. Evolution of body mass in bats: insights from a large supermatrix phylogeny. Journal of Mammalian Evolution 27:123–138.CrossRefGoogle Scholar
Nogueira, M. R., Peracchi, A. L., and Monteiro, L. R.. 2009. Morphological correlates of bite force and diet in the skull and mandible of phyllostomid bats. Functional Ecology 23:715–723.CrossRefGoogle Scholar
Norberg, R. A., and Rayner, J. M. V.. 1987. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London B 316:335–427.Google Scholar
Norberg, U. M., and Fenton, M. B.. 1988. Carnivorous bats? Biological Journal of the Linnean Society 33:383–394.CrossRefGoogle Scholar
Pampush, J. D., Spradley, J. P., Morse, P. E., Harrington, A. R., Allen, K. L., Boyer, D. M., and Kay, R. F.. 2016a. Wear and its effects on dental topography measures in howling monkeys (Alouatta palliata). American Journal of Physical Anthropology 161:705–721.CrossRefGoogle Scholar
Pampush, J. D., Winchester, J. M., Morse, P. E., Vining, A. Q., Boyer, D. M., and Kay, R. F.. 2016b. Introducing molaR: a new R package for quantitative topographic analysis of teeth (and other topographic surfaces). Journal of Mammalian Evolution 23:397–412.CrossRefGoogle Scholar
Pavan, A. C., Martins, F. M., and Morgante, J. S.. 2013. Evolutionary history of bulldog bats (genus Noctilio): recent diversification and the role of the Caribbean in Neotropical biogeography. Biological Journal of the Linnean Society 108:210–224.CrossRefGoogle Scholar
Pineda-Munoz, S., Lazagabaster, I. A., Alroy, J., and Evans, A. R.. 2017. Inferring diet from dental morphology in terrestrial mammals. Methods in Ecology and Evolution 8:481–491.CrossRefGoogle Scholar
Prufrock, K. A., Boyer, D. M., and Silcox, M. T.. 2016a. The first major primate extinction: an evaluation of paleoecological dynamics of North American stem primates using a homology free measure of tooth shape. American Journal of Physical Anthropology 159:683–697.CrossRefGoogle Scholar
Prufrock, K. A., López-Torres, S., Silcox, M. T., and Boyer, D. M.. 2016b. Surfaces and spaces: troubleshooting the study of dietary niche space overlap between North American stem primates and rodents. Surface Topography: Metrology and Properties 4:024005.Google Scholar
Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217–223.CrossRefGoogle Scholar
Rojas, D., Vale, Á., Ferrero, V., and Navarro, L.. 2012. The role of frugivory in the diversification of bats in the Neotropics. Journal of Biogeography 39:1948–1960.CrossRefGoogle Scholar
Rojas, D., Warsi, O. M., and Dávalos, L. M.. 2016. Bats (Chiroptera: Noctilionoidea) challenge a recent origin of extant neotropical diversity. Systematic Biology 65:432–448.CrossRefGoogle ScholarPubMed
Rossoni, D. M., Assis, A. P. A., Giannini, N. P., and Marroig, G.. 2017. Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats. Scientific Reports 7:11076.CrossRefGoogle ScholarPubMed
Rossoni, D. M., Costa, B. M. A., Giannini, N. P., and Marroig, G.. 2019. A multiple peak adaptive 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.CrossRefGoogle ScholarPubMed
Santana, S. E., and Cheung, E.. 2016. Go big or go fish: morphological specializations in carnivorous bats. Proceedings of the Royal Society of London B 283:20160615.Google ScholarPubMed
Santana, S. E., and Portugal, S.. 2016. Quantifying the effect of gape and morphology on bite force: biomechanical modelling and in vivo measurements in bats. Functional Ecology 30:557–565.CrossRefGoogle Scholar
Santana, S. E., Dumont, E. R., and Davis, J. L.. 2010. Mechanics of bite force production and its relationship to diet in bats. Functional Ecology 24:776–784.CrossRefGoogle Scholar
Santana, S. E., Strait, S., and Dumont, E. R.. 2011. The better to eat you with: functional correlates of tooth structure in bats. Functional Ecology 25:839–847.CrossRefGoogle Scholar
Santana, S. E., Grosse, I. R., and Dumont, E. R.. 2012. Dietary hardness, loading behavior, and the evolution of skull form in bats. Evolution 66:2587–2598.CrossRefGoogle ScholarPubMed
Savage, D. E. 1951. A Miocene phyllostomatid Bat from Colombia, South America. Bulletin of the Department of Geology of the University of California 28:357–366.Google Scholar
Schliep, K. P. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593.CrossRefGoogle ScholarPubMed
Self, C. J. 2015. Dental root size in bats with diets of different hardness. Journal of Morphology 276:1065–1074.CrossRefGoogle ScholarPubMed
Selig, K. R., López-Torres, S., Sargis, E. J., and Silcox, M. T.. 2019. First 3D dental topographic analysis of the enamel–dentine junction in non-primate euarchontans: contribution of the enamel–dentine junction to molar morphology. Journal of Mammalian Evolution 26:587–598.CrossRefGoogle Scholar
Selig, K. R., Sargis, E. J., Chester, S. G. B., and Silcox, M. T.. 2020. Using three-dimensional geometric morphometric and dental topographic analyses to infer the systematics and paleoecology of fossil treeshrews (Mammalia, Scandentia). Journal of Paleontology 94:1202–1212.CrossRefGoogle Scholar
Shi, J. J., and Rabosky, D. L.. 2015. Speciation dynamics during the global radiation of extant bats. Evolution 69:1528–1545.CrossRefGoogle ScholarPubMed
Shi, J. J., Westeen, E. P., and Rabosky, D. L.. 2018. Digitizing extant bat diversity: an open-access repository of 3D μCT-scanned skulls for research and education. PLoS ONE 13:e0203022.CrossRefGoogle ScholarPubMed
Simmons, N. B., Seymour, K. L., Habersetzer, J., and Gunnell, G. F.. 2008. Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451:818–821.CrossRefGoogle ScholarPubMed
Simmons, N. B., Seiffert, E. R., and Gunnell, G. F.. 2016. A new family of large omnivorous bats (Mammalia, Chiroptera) from the Late Eocene of the Fayum Depression, Egypt, with comments on use of the name “Eochiroptera.” American Museum Novitates 3857:1–43.CrossRefGoogle Scholar
Simmons, N. B., Gunnell, G. F., and Czaplewski, N. J.. 2020. Fragments and gaps: the fossil record. Pp. 63–86 in Fleming, T. H., Dávalos, L. M., and Mello, M. A. R., eds. Phyllostomid bats: a unique mammalian radiation. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Spradley, J. P., Glazer, B. J., and Kay, R. F.. 2019. Mammalian faunas, ecological indices, and machine-learning regression for the purpose of paleoenvironment reconstruction in the Miocene of South America. Palaeogeography, Palaeoclimatology, Palaeoecology 518:155–171.CrossRefGoogle Scholar
Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'Brien, J., and Murphy, W. J.. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:581–584.CrossRefGoogle ScholarPubMed
Ungar, P. 2004. Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution 46:605–622.CrossRefGoogle ScholarPubMed
Ungar, P. S., Healy, C., Karme, A., Teaford, M., and Fortelius, M.. 2018. Dental topography and diets of platyrrhine primates. Historical Biology 30:64–75.CrossRefGoogle Scholar
Upham, N. S., Ojala-Barbour, R., Brito, J. Velazco, M, P. M., and Patterson, B. D.. 2013. Transitions between Andean and Amazonian centers of endemism in the radiation of some arboreal rodents. BMC Evolutionary Biology 13:191.CrossRefGoogle ScholarPubMed
Vaughan, T. A. 1959. Functional morphology of three bats: Eumops, Myotis, Macrotus. University of Kansas, Lawrence.Google Scholar
Vleut, I., Carter, G. G., and Medellín, R. A.. 2019. Movement ecology of the carnivorous woolly false vampire bat (Chrotopterus auritus) in southern Mexico. PLoS ONE 14:e0220504.CrossRefGoogle Scholar
Wetterer, A. L., Rockman, M. V., and 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 2000:1–200.2.0.CO;2>CrossRefGoogle Scholar
Winchester, J. M., Boyer, D. M., St Clair, E. M., Gosselin-Ildari, A. D., Cooke, S. B., and Ledogar, J. A.. 2014. Dental topography of platyrrhines and prosimians: convergence and contrasts. American Journal of Physical Anthropology 153:29–44.CrossRefGoogle ScholarPubMed
Yohe, L. R., Velazco, P. M., Rojas, D., Gerstner, B. E., Simmons, N. B., and Davalos, L. M.. 2015. Bayesian hierarchical models suggest oldest known plant-visiting bat was omnivorous. Biology Letters 11:20150501.CrossRefGoogle ScholarPubMed
Zuercher, M. E., Monson, T. A., Dvoretzky, R. R., Ravindramurthy, S., and Hlusko, L. J.. 2020. Dental variation in megabats (Chiroptera: Pteropodidae): tooth metrics correlate with body size and tooth proportions reflect phylogeny. Journal of Mammalian Evolution 28:543–558.CrossRefGoogle Scholar