Ecomorphological correlates of inner and middle ear anatomy within phyllostomid bats.


Journal

Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775

Informations de publication

Date de publication:
11 2023
Historique:
revised: 31 01 2023
received: 20 11 2022
accepted: 01 02 2023
medline: 23 10 2023
pubmed: 25 2 2023
entrez: 24 2 2023
Statut: ppublish

Résumé

Echolocation is the primary sense used by most bats to navigate their environment. However, the influence of echolocating behaviors upon the morphology of the auditory apparatus remains largely uninvestigated. While it is known that middle ear ossicle size scales positively with body mass across mammals, and that peak call frequency scales negatively with body mass among bats, there are still large gaps in our understanding of the degree to which allometry or ecology influences the morphology of the chiropteran auditory apparatus. To investigate this, we used μCT datasets to quantify three morphological components of the inner and middle ear: ossicle size, ossicle shape, and cochlear spirality. These data were collected across 27 phyllostomid species, spanning a broad range of body sizes, habitats, and dietary categories, and the relationships between these variables and ear morphology were assessed using a comparative phylogenetic approach. Ossicle size consistently scaled with strong negative allometry relative to body mass. Cochlear spirality was significantly (p = .025) associated with wing aspect ratio (a proxy for habitat use) but was not associated with body mass. From a morphological perspective, the malleus and incus exhibited some variation in kind with diet and call frequency, while stapes morphology is more closely tied to body size. Future work will assess these relationships within other chiropteran lineages, and investigate potential morphological differences in the middle and inner ear of echolocating-vs-non-echolocating taxa.

Identifiants

pubmed: 36823766
doi: 10.1002/ar.25178
doi:

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

2751-2764

Informations de copyright

© 2023 American Association for Anatomy.

Références

Amador, L. I., Almeida, F. C., & Giannini, N. P. (2020). Evolution of traditional aerodynamic variables in bats (Mammalia: Chiroptera) within a comprehensive phylogenetic framework. Journal of Mammalian Evolution, 27(3), 549-561.
Amador, L. I., Simmons, N. B., & Giannini, N. P. (2019). Aerodynamic reconstruction of the primitive fossil bat Onychonycteris finneyi (Mammalia: Chiroptera). Biology Letters, 15(3), 20180857.
Argyle, E. C., & Mason, M. J. (2008). Middle ear structures of Octodon degus (Rodentia: Octodontidae), in comparison with those of subterranean caviomorphs. Journal of Mammalogy, 89(6), 1447-1455.
Bogdanowicz, W., Csada, R. D., & Fenton, M. B. (1997). Structure of noseleaf, echolocation, and foraging behavior in the Phyllostomidae (Chiroptera). Journal of Mammalogy, 78(3), 942-953.
Boyer, D. M., Gunnell, G. F., Kaufman, S., & McGeary, T. M. (2016). Morphosource: Archiving and sharing 3-D digital specimen data. The Paleontological Society Papers, 22, 157-181.
Burnham, K. P., & Anderson, D. R. (2001). Kullback-Leibler information as a basis for strong inference in ecological studies. Wildlife Research, 28(2), 111-119.
Collen, A. (2012). The evolution of echolocation in bats: A comparative approach. University College London.
Crane, M., Silva, I., Grainger, M. J., & Gale, G. A. (2022). Limitations and gaps in global bat wing morphology trait data. Mammal Review, 52(2), 165-176.
Davies, K. T., Maryanto, I., & Rossiter, S. J. (2013). Evolutionary origins of ultrasonic hearing and laryngeal echolocation in bats inferred from morphological analyses of the inner ear. Frontiers in Zoology, 10(1), 1-15.
Dickinson, E., Elminowski, E. E., Flores, D., Eldridge, E. I., Granatosky, M. C., & Hartstone-Rose, A. (2022). A morphological analysis of carnivoran ossicles from Rancho La Brea. Journal of Morphology, 283(10), 1337-1349.
Dumont, E. R., Davalos, L. M., Goldberg, A., Santana, S. E., Rex, K., & Voigt, C. C. (2012). Morphological innovation, diversification and invasion of a new adaptive zone. Proceedings of the Royal Society B: Biological Sciences, 279(1734), 1797-1805.
Farr, M., & Mason, M. (2008). Middle ear morphology in dormice (Rodentia: Gliridae). Mammalian Biology, 73(4), 330-334.
Fleischer, G. (1978). Evolutionary principles of the mammalian middle ear. Advances in Anatomy, Embryology and Cell Biology, 55, 3-69.
Giraud-Sauveur, D. (1969). Recherches biophysiques sur les osselets des cétacés. Mammalia, 3, 285-340.
Gordon, R., Ivens, S., Ammerman, L. K., Fenton, M. B., Littlefair, J. E., Ratcliffe, J. M., & Clare, E. L. (2019). Molecular diet analysis finds an insectivorous desert bat community dominated by resource sharing despite diverse echolocation and foraging strategies. Ecology and Evolution, 9(6), 3117-3129.
Gürbüz, İ., Demiraslan, Y., Dayan, M. O., & Aslan, K. (2019). Morphometric and macroanatomic examination of auditory ossicles in male wolves (Canis lupus). Folia Morphologica, 78(3), 600-605.
Heffner, H. (1983). Hearing in large and small dogs: Absolute thresholds and size of the tympanic membrane. Behavioral Neuroscience, 97(2), 310-318.
Heffner, R., Koay, G., & Heffner, H. (2001). Audiograms of five species of rodents: Implications for the evolution of hearing and the perception of pitch. Hearing Research, 157(1-2), 138-152.
Heffner, R., Koay, G., & Heffner, H. (2006). Hearing in large (Eidolon helvum) and small (Cynopterus brachyotis) non-echolocating fruit bats. Hearing Research, 221(1-2), 17-25.
Hemilä, S., Nummela, S., & Reuter, T. (1995). What middle ear parameters tell about impedance matching and high frequency hearing. Hearing Research, 85(1-2), 31-44.
Houston, R. D., Boonman, A., & Jones, G. (2004). Do echolocation signal parameters restrict bats' choice of prey. In J. A. Thomas, C. F. Moss, & M. Vater (Eds.), Echolocation in bats and dolphins (pp. 339-345). University of Chicago Press.
Huang, G., Rosowski, J., & Peake, W. (2000). Relating middle-ear acoustic performance to body size in the cat family: Measurements and models. Journal of Comparative Physiology A, 186(5), 447-465.
Ives, A. R. (2019). Rs for correlated data: Phylogenetic models, lmms, and glmms. Systematic Biology, 68(2), 234-251.
Jacobs, D. S., Barclay, R. M., & Walker, M. H. (2007). The allometry of echolocation call frequencies of insectivorous bats: Why do some species deviate from the pattern? Oecologia, 152(3), 583-594.
Jones, G., & Barlow, K. E. (2004). Cryptic species of echolocating bats. In J. A. Thomas, C. F. Moss, & M. Vater (Eds.), Echolocation in bats and dolphins. University of Chicago Press.
Kohlsdorf, T., & Navas, C. (2012). Evolution of form and function: Morphophysiological relationships and locomotor performance in tropidurine lizards. Journal of Zoology, 288(1), 41-49.
Kumar, S., Suleski, M., Craig, J. M., Kasprowicz, A. E., Sanderford, M., Li, M., Stecher, G., & Hedges, S. B. (2022). TimeTree 5: An expanded resource for species divergence times. Molecular Biology and Evolution, 39(8), msac174.
Lavender, D., Taraskin, S. N., & Mason, M. J. (2011). Mass distribution and rotational inertia of “microtype” and “freely mobile” middle ear ossicles in rodents. Hearing Research, 282(1-2), 97-107.
Lees, S., Hanson, D. B., & Page, E. A. (1996). Some acoustical properties of the otic bones of a fin whale. The Journal of the Acoustical Society of America, 99(4), 421-2427.
Leiser-Miller, L. B., & Santana, S. E. (2020). Morphological diversity in the sensory system of phyllostomid bats: Implications for acoustic and dietary ecology. Functional Ecology, 34(7), 1416-1427.
Leiser-Miller, L. B., & Santana, S. E. (2021). Functional differences in echolocation call design in an adaptive radiation of bats. Ecology and Evolution, 11(22), 16153-16164.
Linnenschmidt, M., & Wiegrebe, L. (2016). Sonar beam dynamics in leaf-nosed bats. Scientific Reports, 6(1), 1-8.
López-Cuamatzi, I. L., Vega-Gutiérrez, V. H., Cabrera-Campos, I., Ruiz-Sanchez, E., Ayala-Berdon, J., & Saldaña-Vázquez, R. A. (2020). Does body mass restrict call peak frequency in echolocating bats? Mammal Review, 50(3), 304-313.
Mailund, T. (2022). Reformatting tables: tidyr. R 4 Data Science Quick Reference. Springer, pp. 53-75.
Malkemper, E. P., Mason, M. J., & Burda, H. (2020). Functional anatomy of the middle and inner ears of the red fox, in comparison to domestic dogs and cats. Journal of Anatomy, 236(6), 980-995.
Manley, G. A. (2010). An evolutionary perspective on middle ears. Hearing Research, 263(1-2), 3-8.
Manoussaki, D., Chadwick, R. S., Ketten, D. R., Arruda, J., Dimitriadis, E. K., & O'Malley, J. T. (2008). The influence of cochlear shape on low-frequency hearing. Proceedings of the National Academy of Sciences, 105(16), 6162-6166.
Manoussaki, D., Dimitriadis, E., & Chadwick, R. (2006). Cochlea's graded curvature effect on low frequency waves. Physical Review Letters, 96(8), 088701.
Martonos, C., Gudea, A., Lațiu, C., Blagojevic, M., & Stan, F. (2022). Morphological and morphometrical aspects of the auditory ossicles in the European badger (Meles Meles). Veterinary Sciences, 9(9), 483.
Mason, M. (2001). Middle ear structures in fossorial mammals: A comparison with non-fossorial species. Journal of Zoology, 255(4), 467-486.
Mason, M. (2013). Of mice, moles and Guinea pigs: Functional morphology of the middle ear in living mammals. Hearing Research, 301, 4-18.
Mason, M. (2016). Structure and function of the mammalian middle ear. I: Large middle ears in small desert mammals. Journal of Anatomy, 228(2), 284-299.
Norberg, U. M., & Rayner, J. M. (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, Biological Sciences, 316(1179), 335-427.
Nummela, S. (1995). Scaling of the mammalian middle ear. Hearing Research, 85(1-2), 18-30.
Nummela, S., Wagar, T., Hemila, S., & Reuter, T. (1999). Scaling of the cetacean middle ear. Hearing Research, 133, 71-81.
Olsen, A. M. (2017). Feeding ecology is the primary driver of beak shape diversification in waterfowl. Functional Ecology, 31(10), 1985-1995.
Orliac, M., & Billet, G. (2016). Fallen in a dead ear: Intralabyrinthine preservation of stapes in fossil artiodactyls. Palaeovertebrata, 40(1), e3.
Polly, P. D., Lawing, A. M., Fabre, A.-C., & Goswami, A. (2013). Phylogenetic principal components analysis and geometric morphometrics. Hystrix, 24(1), 33.
Ravicz, M. E., Rosowski, J. J., & Voigt, H. F. (1992). Sound-power collection by the auditory periphery of the Mongolian gerbil M erionesunguiculatus. I: Middle-ear input impedance. The Journal of the Acoustical Society of America, 92(1), 157-177.
Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution, 63(12), 3258-3268.
Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217-223.
Rex, K., Czaczkes, B. I., Michener, R., Kunz, T. H., & Voigt, C. C. (2010). Specialization and omnivory in diverse mammalian assemblages. Ecoscience, 17(1), 37-46.
Rosowski, J. J. (1992). Hearing in transitional mammals: Predictions from the middle-ear anatomy and hearing capabilities of extant mammals. In D. B. Webster, R. R. Fay, & A. N. Popper (Eds.), The evolutionary biology of hearing (pp. 615-631). Springer.
Salih, W. H., Buytaert, J. A., Aerts, J. R., Vanderniepen, P., Dierick, M., & Dirckx, J. J. (2012). Open access high-resolution 3D morphology models of cat, gerbil, rabbit, rat and human ossicular chains. Hearing Research, 284(1-2), 1-5.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671-675.
Schnitzler, H.-U., & Kalko, E. K. (2001). Echolocation by insect-eating bats: We define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. Bioscience, 51(7), 557-569.
Sidorkewicj, N. S., & Casanave, E. B. (2012). Morfología del oído medio en tres especies de armadillos (Dasypodidae, Xenarthra) de Argentina. International Journal of Morphology, 30(4), 1500-1507.
Stoessel, A., David, R., Gunz, P., Schmidt, T., Spoor, F., & Hublin, J.-J. (2016). Morphology and function of Neandertal and modern human ear ossicles. Proceedings of the National Academy of Sciences, 113(41), 11489-11494.
Stoffberg, S., Jacobs, D. S., & Matthee, C. A. (2011). The divergence of echolocation frequency in horseshoe bats: Moth hearing, body size or habitat? Journal of Mammalian Evolution, 18(2), 117-129.
Strickler, T. L. (1973). The functional morphology of the pectoral girdle muscles in the Chiroptera. University of Chicago.
Thiagavel, J., Santana, S. E., & Ratcliffe, J. M. (2017). Body size predicts echolocation call peak frequency better than gape height in vespertilionid bats. Scientific Reports, 7(1), 1-6.
Vanderelst, D., De Mey, F., Peremans, H., Geipel, I., Kalko, E., & Firzlaff, U. (2010). What noseleaves do for FM bats depends on their degree of sensorial specialization. PLoS One, 5(8), e11893.
Varzinczak, L. (2020). Understanding the relationship between climatic niches and dispersal through the lens of bat wing morphology. Journal of Zoology, 312(4), 239-247.
Voss, S. E., & Allen, J. B. (1994). Measurement of acoustic impedance and reflectance in the human ear canal. The Journal of the Acoustical Society of America, 95(1), 372-384.
Wible, J. R., & Spaulding, M. (2012). A reexamination of the Carnivora malleus (Mammalia, Placentalia). PLoS One, 7(11), e50485.
Wickham, H. (2016). Data analysis. ggplot2. Springer, pp. 189-201.
Wickham, H., François, R., Henry, L., & Müller, K. (2015). dplyr: A grammar of data manipulation. R package version 04 3, p. 156.
Wilkins, K. T., Roberts, J. C., Roorda, C. S., & Hawkins, J. E. (1999). Morphometrics and functional morphology of middle ears of extant pocket gophers (Rodentia: Geomyidae). Journal of Mammalogy, 80(1), 180-198.
Wilson, D., & Mittermeier, R. (2020). Handbook of the mammals of the world. Vol. 9: Bats. Lynx Edicions.
Wilson, J., & Bruns, V. (1983). Middle-ear mechanics in the CF-bat Rhinolophus ferrumequinum. Hearing Research, 10(1), 1-13.
Zala, S. M., Reitschmidt, D., Noll, A., Balazs, P., & Penn, D. J. (2017). Sex-dependent modulation of ultrasonic vocalizations in house mice (Mus musculus musculus). PLoS One, 12(12), e0188647.

Auteurs

Edwin Dickinson (E)

Department of Anatomy, New York Institute of Technology, Old Westbury, New York, USA.

Emily Tomblin (E)

Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA.

Madison Rose (M)

Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA.
Department of Anthropology, University of Toronto, Toronto, Ontario, Canada.

Zoe Tate (Z)

Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA.

Mihika Gottimukkula (M)

Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA.

Michael C Granatosky (MC)

Department of Anatomy, New York Institute of Technology, Old Westbury, New York, USA.

Sharlene E Santana (SE)

Department of Biology and Burke Museum of Natural History and Culture, University of Washington, Seattle, Washington, USA.

Adam Hartstone-Rose (A)

Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA.

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