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Myology of the Head, Neck, and Thoracic Region of the Lesser Grison (Galictis cuja) in Comparison with the Red Panda (Ailurus fulgens) and Other Carnivorans: Phylogenetic and Functional Implications

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Abstract

The lesser grison (Galictis cuja) and the red panda (Ailurus fulgens) represent two opposed morpho-functional musteloid extremes. The mid-sized lesser grison is primarily terrestrial, a frequent burrow-dweller, and carnivorous, while the larger, scansorial red panda eats bamboo. This study documents the axial myology of these species, including muscle descriptions, weights, and optimizations. Muscle maps are also provided for the lesser grison, representing the first axial maps for a wild-caught carnivoran. The functional analyses revealed that G. cuja, contrary to A. fulgens, possesses longer, stronger, and subdivided neck muscles. It also possesses a thoraco-lumbar iliocostalis system that is more developed than the longissimus complex, and numerous, robust, and laterally inserted deep bellies of the cervical and thoracic transversospinalis systems. These specializations allow powerful neck movement during hunting and transport of heavy prey as well as axial flexibility, facilitating bounding gaits and lateral movements while navigating subterranean galleries. Some myological traits of the red panda differ from those expected in a highly herbivorous taxon (e.g., m. sternocephalicus, m. masseter), and may reflect its depredatory ancestry. The optimization analysis revealed phylogenetically informative traits across Carnivora, including the absence of m. longissimus capitis in Mephitidae, the absence of spinous thoracic origins for m. biventer cervicis in Musteloidea, and the presence of a relatively lateral insertion of m. rectus dorsalis capitis intermedius in the clade Ictonychinae+Lutrinae+Mustelinae. This study reveals key associations between axial myological and osteological features that will prove useful for future studies of carnivorans.

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Acknowledgments

We thank Editor-in-Chief John R. Wible, Rui Diogo, and one anonymous reviewer for their valuable comments that improved this work. R.E.F. thanks Jim Mead and Richard Thorington (National Museum of Natural History, Smithsonian Institution) for granting permission to work on the red panda specimens, Linda Gordon, Dave Schmidt, and Helen Kafka (National Museum of Natural History, Smithsonian Institution) for facilitating the shipment of the specimens to Arizona, and Charles Potter and John Ososky (National Museum of Natural History, Smithsonian Institution) for their support. M.D.E. thanks Francisco J. Prevosti for providing materials and ideas, and David Flores and Sergio Lucero (Museo Argentino de Ciencias Naturales) for granting access to the lesser grison specimens. R.E.F. thanks Linda Walters (Midwestern University) for assisting with the dissection of USNM 597647, Paul Boehmer (University of Arizona College of Medicine Phoenix) for assistance in translating Carlsson (1925), and Shawn Zack (University of Arizona College of Medicine Phoenix) for fruitful discussions. M.D.E. thanks Marcela Deborah Huerta de la Rocha, Sergio Lucero, Santiago Nenda, Mariella Superina, Maximiliano Álvarez, and Mariano Ramírez for their recommendations and collaboration; and Daria Wingreen-Mason, Cynthia Lamb, Anna Perepelova, César García-Esponda, Robert Scapino, Susanne Whitaker, Eric Yensen, Donald Quaife, Anthony Russell, Alberto Valenciano Vaquero, the Biodiversity Heritage Library, and the Flower-Sprecher Veterinary Library of Cornell University, for their help in bibliographic research. The figures of Ailurus fulgens were produced by Brent Adrian, while those for Galictis cuja were created by Marcos D. Ercoli. Funding for this project was provided by a Midwestern University Research Grant (R.E.F.) and the “Osvaldo Reig” (grant to M.D.E.) from the Sociedad Argentina para el Estudio de los Mamíferos (SAREM).

Author Contributions

M.D.E., R.E.F.: Concept and design. M.D.E., A.A., F.B., M.M.M., E.J., H.F.S., B.A., M.B., K.B., M.P., M.S., R.W., and R.E.F.: Data collection and analysis. M.D.E., A.A., and R.E.F: Draft of manuscript. M.D.E., A.A., F.B., M.M.M., E.J., H.F.S., B.A. and R.E.F.: Approval of manuscript. M.D.E., A.A., B.A., and R.E.F.: Design of figures and tables.

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Authors and Affiliations

  1. CONICET, San Salvador de Jujuy, Argentina

    Marcos D. Ercoli, Alicia Álvarez, Felipe Busker & Miriam M. Morales

  2. División Mastozoología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Buenos Aires, C1405DJR, Argentina

    Marcos D. Ercoli & Alicia Álvarez

  3. Instituto de Ecorregiones Andinas (INECOA), Universidad Nacional de Jujuy, CONICET, IdGyM, Av. Bolivia 1661, Y4600GNE, San Salvador de Jujuy, Jujuy, Argentina

    Marcos D. Ercoli & Alicia Álvarez

  4. Instituto de Geología y Minería (IdGyM), Universidad Nacional de Jujuy, Av. Bolivia 1661, San Salvador de Jujuy, Y4600GNE, Argentina

    Marcos D. Ercoli & Alicia Álvarez

  5. Instituto Patagónico de Geología y Paleontología, Centro Nacional Patagónico, Puerto Madryn, U9120AOU, Chubut, Argentina

    Felipe Busker

  6. CIT-Jujuy. Centro de Estudios Territoriales Ambientales y Sociales, Facultad de Ciencias Agrarias, Universidad Nacional de Jujuy, San Salvador de Jujuy, Y4600DTA, Argentina

    Miriam M. Morales

  7. School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA

    Emily Julik, Mike Barton, Keerthi Bhagavatula, Meifawn Poole, Matt Shahsavan, Rachel Wechsler & Rebecca E. Fisher

  8. Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, Glendale, AZ, 85308, USA

    Heather F. Smith & Brent Adrian

  9. Department of Basic Medical Sciences, The University of Arizona College of Medicine-Phoenix, Phoenix, AZ, 85004, USA

    Rebecca E. Fisher

Authors
  1. Marcos D. Ercoli
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  2. Alicia Álvarez
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  3. Felipe Busker
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  4. Miriam M. Morales
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  5. Emily Julik
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  6. Heather F. Smith
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  7. Brent Adrian
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  8. Mike Barton
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  9. Keerthi Bhagavatula
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  10. Meifawn Poole
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  11. Matt Shahsavan
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  12. Rachel Wechsler
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  13. Rebecca E. Fisher
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Corresponding author

Correspondence to Marcos D. Ercoli.

Electronic supplementary material

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Appendix S1

Myological description of the caudal region of Ailurus fulgens (PDF 36.4 kb)

Fig. S1

Dorsal view of the tail muscles in Ailurus fulgens (PDF 933 kb)

Fig. S2

Diagram showing the caudal vertebrae in Ailurus fulgens and the tendon variation of m. sacrocaudalis dorsalis lateralis on the left and right sides of specimen USNM 525292 (dorsal view) (PDF 31.9 kb)

Fig. S3

Lateral view of the tail muscles in Ailurus fulgens (PDF 735 kb)

Fig. S4

Ventral view of the tail muscles in Ailurus fulgens. M. coccygeus is figured on the right side only, while the components of the m. levator ani are illustrated on the left side only. (PDF 1.19 mb)

Fig. S5

Muscle character definitions and optimization onto a combined phylogeny (after Flynn et al. 2005; Koepfli et al. 2007, 2008; Sato et al. 2012). Plain colors represent unambiguous states, dashed bi- or tri-colored lines indicate ambiguous states, and plain gray line indicates unknown or non-applicable state. The data sources are summarized in Table 1 and the text. (PDF 66.6 kb)

Table S1

Dehydrated muscle mass data (in milligrams, mg) of the axial musculature of Galictis cuja (specimens: S.1 = MACN-Ma 25483, male; and S.2 = MACN-Ma 28.163, female), left (L) and right (R) side. “-“ indicates that the corresponding muscle was measured as many subunits or included in a group of muscles elsewhere in the table; no mark indicates that the muscle was absent; and “?” indicates missing data. Italics indicate terms not present in the Nomina Anatomica Veterinaria (Waibl et al. 2005) (PDF 88.0 kb)

Table S2

Muscle mass data (in grams, g) of the axial musculature of a female specimen of Ailurus fulgens (USNM 525292; left side). A number of muscles were not measured due to damage incurred during necropsy or the small size of some muscles and the relative sensitivity of the scale that was available. Italics indicate terms not present in the Nomina Anatomica Veterinaria (Waibl et al. 2005) (PDF 110 kb)

Table S3

Intraspecific variation observed in the two specimens of Galictis cuja analyzed (left and right sides). “x” indicates side and specimen where the feature described is present, no marks indicates absence of the feature, and “?” indicates missing data (PDF 199 kb)

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Ercoli, M.D., Álvarez, A., Busker, F. et al. Myology of the Head, Neck, and Thoracic Region of the Lesser Grison (Galictis cuja) in Comparison with the Red Panda (Ailurus fulgens) and Other Carnivorans: Phylogenetic and Functional Implications. J Mammal Evol 24, 289–322 (2017). https://doi.org/10.1007/s10914-016-9339-8

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