Skip to main content
SpringerLink
Log in

Exploration of the morphology and functional implications of the forelimb in bats (Mammalia, Chiroptera) from the Neotropical region

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

A Correction to this article was published on 02 March 2023

This article has been updated

Abstract

The active flight allows bats to explore different ecological niches, resulting in diverse feeding habits and great morphological variation. Studies using biomechanical indices to explore the relationships between forelimb skeletal morphology and ecological aspects are scarce in bats. For this reason, we decided to analyze, in a functional context, the relationship between forelimb morphology and feeding ecology of Neotropical bats. To describe the morphology of the forelimbs, we used six biomechanical indices, and evaluated their correlation with foraging habitats and trophic guilds in five families of bats distributed in the Neotropical region. We examined 140 specimens belonging to 23 genera and 43 extant species. Among the morpho-functional indices analyzed, the epicondylar index, the humeral robustness, and the radial distal end width index were the variables that most contributed to the discriminant functions. Our results showed a direct correlation between forelimb morphology and foraging habitats, which could indicate that these morphological characteristics are possibly shared, despite the different evolutionary histories in the analyzed taxa. Here, we provide new morpho-functional and biomechanical data that will facilitate the evaluation of the evolution of morphological diversification in bats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Calculations and analyses are published in this article and its supplementary information files, raw data may be made available upon request to the authors.

Change history

References

  • Adams RA, Carter RT (2017) Megachiropteran bats profoundly unique from microchiropterans in climbing and walking locomotion: evolutionary implications. PLoS ONE 12(9):e0185634. https://doi.org/10.1371/journal.pone.0185634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adams RA, Shaw JB (2013) Time’s arrow in the evolutionary development of bat flight. In: Adams RA, Pedersen SC (eds) Bat evolution, ecology, and conservation. Springer, New York, pp 21–46

    Chapter  Google Scholar 

  • Aguirre LF (2002) Structure of a Neotropical savanna bat community. J Mammal 83:775–784

    Article  Google Scholar 

  • Amador LI, Simmons NB, Giannini NP (2019) Aerodynamic reconstruction of the primitive fossil bat Onychonycteris finneyi (Mammalia: Chiroptera). Biol Lett 15:20180857

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson SC, Ruxton GD (2020) The evolution of flight in bats: a novel hypothesis. Mammal Rev 50:426–439

    Article  Google Scholar 

  • Argot C (2001) Functional-Adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J Morph 247:51–79

    Article  CAS  PubMed  Google Scholar 

  • Arita HT, Fenton MB (1997) Flight and echolocation in the ecology and evolution of bats. Trends Ecol Evol 12:53–58

    Article  CAS  PubMed  Google Scholar 

  • Barquez RM (1987) Los murciélagos de Argentina. Doctoral thesis, Universidad Nacional de Tucumán, Tucumán. Argentina.

  • Bishop KL (2008) The evolution of flight in bats: narrowing the field of plausible hypotheses. Q Rev Biol 83:153–169

    Article  PubMed  Google Scholar 

  • Czaplewski NJ, Morgan GS, McLeod SA (2007) Chiroptera. In: Janis CM, Gunnell GF, Uhen MD (eds) Evolution of tertiary mammals of North America. Cambridge University Press, Cambridge, pp 174–197

    Google Scholar 

  • Denzinger A, Schnitzler HU (2013) Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Front Physiol 4:1–15

    Article  Google Scholar 

  • Dobson GE (1878) Catalogue of the Chiroptera in the collection of the British museum. Taylor and Francis Limited, London

    Google Scholar 

  • Elissamburu A, Vizcaíno SF (2004) Limb proportions and adaptations in caviomorph rodents (Rodentia: Caviomorpha). J Zool 262:145–159

    Article  Google Scholar 

  • Freeman PW (1981) Correspondence of food habits and morphology in insectivorous bats. J Mammal 62:166–173

    Article  Google Scholar 

  • Freeman PW (2000) Macroevolution in microchiroptera: recoupling morphology and ecology with phylogeny. Evol Ecol Res 2:317–335

    Google Scholar 

  • Freeman PW, Lemen CA (1992) Puncturing ability of idealized canine teeth: edged and nonedged shanks. J Zool 269:51–56

    Article  Google Scholar 

  • Gaudioso PJ (2019) Morfología y morfometría del esqueleto postcraneal de murciélagos (Mammalia: Chiroptera) de Argentina. Publicaciones Especiales N° 2, PIDBA (Programa de Investigaciones de Biodiversidad Argentina), San Miguel de Tucumán.

  • Gaudioso PJ, Martínez JJ, Barquez RM, Díaz MM (2020) Evolution of scapula shape in several families of bats (Chiroptera. Mammalia). J Zool Syst Evol Res 58:1374–1394

    Article  Google Scholar 

  • Gálvez-López E (2021) Quantifying morphological adaptations using direct measurements: The carnivoran appendicular skeleton as a case study. Anat Rec 304:480–506

    Article  Google Scholar 

  • Giannini NP (2012) Toward an integrative theory on the origin of bat flight. In: Gunnell GF, Simmons NB (eds) Evolutionary history of bats: fossils, molecules and morphology. Cambridge University Press, Cambridge, pp 353–384

    Chapter  Google Scholar 

  • Giannini NP, Gunnell GF, Habersetzer J, Simmons NB (2012) Early evolution of body size in bats. In: Gunnell GF, Simmons NB (eds) Evolutionary history of bats: fossils, molecules and morphology. Cambridge University Press, Cambridge, pp 530–555

    Chapter  Google Scholar 

  • Greene WE (1951) The development of the carpal bones in the bat. J Morphol 89:409–422

    Article  Google Scholar 

  • Guillén-Servent A, Ibáñez C (2007) Unusual echolocation behavior in a small Molossid bat, Molossops temminckii, that forages near background clutter. Behav Ecol Sociobiol 61:1599–1613

    Article  Google Scholar 

  • Gunnell GF, Simmons NB (2005) Fossil evidence and the origin of bats. J Mammal Evol 12:209–246

    Article  Google Scholar 

  • Hand SJ, Weisbecker V, Beck RMD, Archer M, Godthelp H, Tennyson AJD, Worthy TH (2009) Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand’s endemic mystacinids. BMC Evol Biol 9:169

    Article  PubMed  Google Scholar 

  • Hildebrand M (1985) Digging of quadrupeds. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Harvard University Press, Cambridge, pp 89–109

    Chapter  Google Scholar 

  • Hill JE, Smith JD (1984) Bats: a natural history. University of Texas Press, Austin

    Google Scholar 

  • Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristics and statistical approaches. Ecology 74:2204–2214

    Article  Google Scholar 

  • Jepsen GL (1966) Early Eocene bat from Wyoming. Science 154:1333–1338

    Article  CAS  PubMed  Google Scholar 

  • Jullien R (1969) Interprétation des surfaces articulaires du coude des chiroptères. Mammalia 33:659–665

    Article  Google Scholar 

  • Klingenberg CP, Zimmermann M (1992) Static, ontogenetic, and evolutionary allometry: a multivariate comparison in nine species of water striders. Am Naturalist 140:601–620

    Article  Google Scholar 

  • Kovalyova IM (2014) Key morphofunctional transformations in the evolution of bats (Mammalia, Chiroptera). Russ J Dev Biol 45:324–336

    Article  Google Scholar 

  • Lessa EP, Vasallo AI, Verzi DH, Mora MS (2008) Evolution of morphological adaptations for digging in living and extinct ctenomyid and octodontid rodents. The Linnean Society of London. Biol J Linn Soc 95:267–283

    Article  Google Scholar 

  • Lim BK, Engstrom MD, Reid FA, Simmons NB, Voss RS, Fleck DW (2010) A New species of Peropteryx (Chiroptera: Emballonuridae) from Western Amazonia with comments on phylogenetic relationships within the genus. Am Mus Novit 3686:1–20

    Article  Google Scholar 

  • López-Aguirre C, Hand SJ, Koyabu D, Tu VT, Wilson LA (2020) Phylogeny and foraging behaviour shape modular morphological variation in bat humeri. J Anat 238:1312–1329

    Article  PubMed  Google Scholar 

  • López-Aguirre C, Wilson LAB, Koyabu D, Tan Tu VT, Hand SJ (2021) Variation in cross-sectional shape and biomechanical properties of the bat humerus under Wolff’s law. Anat Rec 304:1937–1952. https://doi.org/10.1002/ar.24620

    Article  Google Scholar 

  • Miller GS Jr (1907) The families and genera of bats. Bull US Natl Mus 57:1–282

    Google Scholar 

  • Montoya-Sanhueza G, Bennett NC, Chinsamy A, Šumbera R (2022) Functional anatomy and disparity of the postcranial skeleton of African mole-rats (Bathyergidae). Front Ecol Evol 10:857474

    Article  Google Scholar 

  • Moretto L, Lim BK, Cadenillas R, Martínez JR (2017) Analysis of bat humeri from Late Pleistocene Talara Tar Seeps of northwestern Peru, with paleoenvironmental implications. J Vertebr Paleontol 37:e1250097

    Article  Google Scholar 

  • Moyers Arévalo RL, Amador LI, Almeida FC, Giannini NP (2020) Evolution of body mass in bats: insights from a large supermatrix phylogeny. J Mammal Evol 27:123–138. https://doi.org/10.1007/s10914-018-9447-8

    Article  Google Scholar 

  • Norberg UM (1972) Functional osteology and myology of the wing of the dog-faced bat Rousettus aegyptiacus (E. Geoffroy) (Mammalia, Chiroptera). Zeitschrift Für Morphologie Der Tiere 73:1–44

    Article  Google Scholar 

  • Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia:Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans Royal Soc B 316:335–427

    Google Scholar 

  • O´Sullivan JA (1995) Skeletal indicators of arboreal and terrestrial positional behavior in didelphid marsupials. MA thesis, Hunter College, City University of New York, United States of America.

  • Oksanen JF, et al. (2018) vegan: Community ecology package, R package version 1.15–4.

  • Olson RA, Womble MD, Thomas DR, Glenn ZD, Butcher MT (2016) Functional morphology of the forelimb of the nine-banded armadillo (Dasypus novemcinctus): comparative perspectives on the myology of Dasypodidae. J Mammal Evol 23:49–69. https://doi.org/10.1007/s10914-015-9299-4

    Article  Google Scholar 

  • Panyutina AA (2020) Adaptationist approach to construction of evolutionary scenarios. Mammalian flapping flight as an example. In: Zeller U, Perry G, Starik N, Göttert T (eds) Organisms in nature—evolutionary perspective and ecological significance. Humboldt-Universität zu Berlin, Berlin, pp 29–41

    Google Scholar 

  • Panyutina AA, Korzun LP, Kuznetsov AN (2015) Flight of mammals from terrestrial limbs to wings. Springer, New York

    Book  Google Scholar 

  • Papadimitriou HM, Swartz SM, Kunz TH (1996) Ontogenetic and anatomic variation in mineralization of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis. J Zool 240:411–426

    Article  Google Scholar 

  • Pérez MJ, Barquez RM, Díaz MM (2017) Morphology of the limbs in the semi-fossorialdesert rodent species of Tympanoctomys (Octodontidae, Rodentia). ZooKeys 710:77–96

    Article  Google Scholar 

  • Pérez MJ, Cassini GH, Díaz MM (2021) The forelimbs of Octodontidae (Rodentia: Mammalia): substrate use, morphology, and phylogenetic signal. Zool 144:125879

    Article  Google Scholar 

  • Popov I (2005) An enigma for evolutionary theory. The Origin of Bats Ludus Vitalis 8:4–19

    Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Rose J, Moore A, Russell A, Butcher M (2014) Functional osteology of the forelimb digging apparatus of badgers. J Mammal 95:543–558

    Article  Google Scholar 

  • Rossoni DM, Costa BMA, Giannini NP, 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. Evol 73:961–981

    Article  Google Scholar 

  • Safi K, Meiri S, Jones KE (2013) Evolution of body size in bats. In: Smith FA, Lyons SK (eds) Animal body size: linking pattern and process across space, time, and taxonomic group. University of Chicago Press, Chicago and London, pp 95–115

    Chapter  Google Scholar 

  • Salton JA, Sargis EJ (2008) Evolutionary Morphology of the Tenrecoidea (Mammalia) Forelimb Skeleton. In: Sargis EJ, Dagosto M (eds) Mammalian evolutionary morphology. Vertebrate paleobiology and paleoanthropology. Springer, Netherlands, pp 51–71

    Google Scholar 

  • Samuels JX, Van Valkenburgh B (2008) Skeletal indicators of locomotor adaptations in living and extinct rodents. J Morphol 269:1387–1411

    Article  PubMed  Google Scholar 

  • Samuels JX, Meachen JA, Sakai SA (2012) Postcranial morphology and the locomotor habits of living and extinct carnivorans. J Morphol 274:121–146

    Article  PubMed  Google Scholar 

  • Sánchez MS, Carrizo LV (2021) Forelimb bone morphology and its association with foraging ecology in four families of neotropical bats. J Mammal Evol 28:99–110. https://doi.org/10.1007/s10914-020-09526-5

    Article  Google Scholar 

  • Sargis EJ (2002) Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J Morphol 253:10–42

    Article  PubMed  Google Scholar 

  • Sargis EJ, Szalay FS (2001) Model based analysis of postcranial osteology of marsupials from the Palaeocene of Itaboraí (Brazil) and the phylogenetics and biogeography of Metatheria. Geodiversitas 23:139–302

    Google Scholar 

  • Sarmiento EE (1988) Anatomy of the Hominoid wrist joint: its evolutionary and functional implications. Int J Primatol 9:281–345

    Article  Google Scholar 

  • Schnitzler HU, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394

    Article  Google Scholar 

  • Simmons NB, Geisler JH (1998) Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in microchiroptera. Bull Am Mus Nat Hist 235:1–182

    Google Scholar 

  • Smith JD (1972) Systematics of the chiropteran family mormoopidae. Misc Publ Univ Kansas Mus Nat Hist 56:1–132

    Google Scholar 

  • Smith JD, Starrett A (1979) Morphometric analysis of chiropteran wings. In: Baker RJ, Jones JKJ, Carter DC (eds) Biology of the bats of the new world family phyllostomatidae, Part III. Special Publications, The Museum of Texas Tech University, Lubbock, pp 1–441

    Google Scholar 

  • Smith KK, Redford KH (1990) The anatomy and function of the feeding apparatus in two armadillos (Dasypoda): anatomy is not destiny. J Zool Lond 222:27–47

    Article  Google Scholar 

  • Speakman JR (2001) The evolution of flight and echolocation in bats: another leap in the dark. Mammal Rev 31:111–130

    Article  Google Scholar 

  • Strauss RE (2010) Discriminating groups of organisms. In: Elewa A (ed) Morphometrics for nonmorphometricians. Springer, Berlin, pp 73–91

    Chapter  Google Scholar 

  • Strickler TL (1978) Functional osteology and myology of the shoulder in the Chiroptera. In: Hecht MK, Szalay FS (eds) Contributions to vertebrate evolution. Karger, New York, pp 1–198

    Google Scholar 

  • Swartz SM (1997) Allometric patterning in the limb skeleton of bats: implications for the mechanics and energetics of powered flight. J Morphol 234:277–294

    Article  PubMed  Google Scholar 

  • Swartz SM, Middleton KM (2008) Biomechanics of the bat limb skeleton: scaling, material properties and mechanics. Cells Tissues Organs 187:59–84

    Article  PubMed  Google Scholar 

  • Swartz SM, Bennett MB, Carrier DR (1992) Wing bone stresses in free flying bats and the evolution of skeletal design for flight. Nature 359:726–729

    Article  CAS  PubMed  Google Scholar 

  • Swartz SM, Iriarte-Díaz J, Riskin DK, Breuer KS (2012) A bird? A plane? No, it’s a bat: an introduction to the biomechanics of bat flight. In: Gunnell GF, Simmons NB (eds) Evolutionary history of bats: fossils, molecules and morphology. Cambridge University Press, Cambridge, pp 317–352

    Chapter  Google Scholar 

  • Toledo N (2016) Paleobiological integration of Santacrucian sloths (early Miocene Xenarthra: Dasypodidae). J Zool Lond 257:117–127

    Google Scholar 

  • Vaughan TA (1959) Functional morphology of three bats: Eumops, Myotis, Macrotus. Publ Mus Nat Hist Univ Kansas 12:1–153

    Google Scholar 

  • Vaughan TA (1970) The skeletal system. In: Wimsatt WA (ed) Biology of bats. Academic Press Inc., New York, pp 98–139

    Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • Vizcaíno SF, Bargo MS (2021) Views on the form-function correlation and biological design. J Mammal Evol 28:15–22

    Article  Google Scholar 

  • Vizcaíno SF, Milne N (2002) Structure and function in armadillo limbs (Mammalia: Xenarthra: Dasypodidae). J Zool 257:117–127

    Article  Google Scholar 

  • Walton DW, Walton GM (1970) Postcranial osteology of bats. In: Slaugther BH, Walton DW (eds) About bats. Southern Methodist University Press, Dallas, pp 93–126

    Google Scholar 

  • Warton DI, Weber NC (2002) Common slope tests for bivariate errors-in-variables models. Biom J 44:161–174

    Article  Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  • Yalden DW (1966) The anatomy of mole locomotion. J Zool Lond 149:55–64

    Article  Google Scholar 

  • Yalden DW (1970) The functional morphology of the carpal bones in carnivores. Acta Anat 77:481–500

    Article  CAS  PubMed  Google Scholar 

  • Yalden DW (1971) The functional morphology of the carpus in ungulate mammals. Acta Anat 78:461–487

    Article  CAS  PubMed  Google Scholar 

  • Yalden DW (1972) The form and function of the carpal bones in some arboreally adapted mammals. Acta Anat 82:383–406

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Rubén Barquez, curator of the Colección Mamíferos Lillo–Universidad Nacional de Tucumán. This work was supported by a doctoral fellowship of CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) awarded to PJG and Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación, PICT-2016-0359 granted to MMD. The author PJG thanks Guillermina Krieger and Marilina Sobrero for their help in writing the manuscript, and Rubén Barquez for revising and improving the English.

Funding

Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación, UNT PICT 2016-0359.

Author information

Authors and Affiliations

  1. Instituto de Investigaciones de Biodiversidad Argentina (PIDBA), Programa de Conservación de los Murciélagos de Argentina (PCMA), Facultad de Ciencias Naturales e IML, Universidad Nacional de Tucumán. Miguel Lillo 205, 4000, Tucumán, Argentina

    Pablo J. Gaudioso, M. Julieta Pérez, Santiago Gamboa Alurralde & M. Mónica Díaz

  2. Centro Científico Tecnológico del Consejo Nacional de Investigaciones Científicas y Técnicas (CCT CONICET NOA Sur), Crisóstomo Álvarez 722, 4000, Tucumán, Argentina

    Pablo J. Gaudioso, M. Julieta Pérez, Néstor Toledo & M. Mónica Díaz

  3. Instituto de Ambiente de Montaña y Regiones Áridas (IAMRA), Universidad Nacional de Chilecito, Julián Amatte 22, 5360, La Rioja, Argentina

    Pablo J. Gaudioso

  4. División Paleontología Vertebrados, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, 122 y 60, 1900, Buenos Aires, Argentina

    Néstor Toledo

  5. Fundación Miguel Lillo. Miguel Lillo 251, 4000, Tucumán, Argentina

    M. Mónica Díaz

Authors
  1. Pablo J. Gaudioso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Julieta Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santiago Gamboa Alurralde
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Néstor Toledo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Mónica Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Gaudioso PJ, Pérez MJ and Gamboa Alurralde S wrote the main manuscript text and prepared figures 1-7. Gaudioso PJ and Pérez MJ processed the data and interpreted the results. Diaz MM and Toledo N revised the English in the entire manuscript and supervised the findings of this research. All authors discussed the results and reviewed the final manuscript.

Corresponding author

Correspondence to M. Julieta Pérez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: Corrected version of table 1 and data availability statement updated.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 31 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gaudioso, P.J., Pérez, M.J., Gamboa Alurralde, S. et al. Exploration of the morphology and functional implications of the forelimb in bats (Mammalia, Chiroptera) from the Neotropical region. Zoomorphology 142, 233–249 (2023). https://doi.org/10.1007/s00435-022-00588-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-022-00588-y

Keywords

Search

Navigation