Skip to main content
Log in

Myology of the Feeding Apparatus of Myrmecophagid Anteaters (Xenarthra: Myrmecophagidae)

  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The musculoskeletal feeding apparatus of anteaters in the family Myrmecophagidae (Eutheria: Xenarthra) is described, compared among the three extant genera (Tamandua, Myrmecophaga, Cyclopes), and interpreted in a phylogenetic framework. Character polarities are assessed with reference to other xenarthrans, eutherians, and didelphid marsupials. Xenarthrans are widely regarded as basal eutherians, and this is reflected in the apparent retention of plesiomorphic character states in jaw and pharyngeal musculature. Jaw closing muscles are architecturally simple, the stylohyoideus is absent, the stylopharyngeus is robust and architecturally complex, and the superior pharyngeal constrictor is weak. At the same time, the highly specialized trophic ecology of myrmecophagids is reflected in derived features of the jaw, tongue, and palatal musculature. The sternomandibularis is present, the tongue is largely composed of a sternog-lossus with no attachments to the hyoid apparatus, other glossus muscles are modified and do not enter the tongue, and the mylohyoideus and stylopharyngeus contribute to the soft palate, while other palatal muscles vary among the myrmecophagid genera. Feeding apparatus mycology provides further support for myrmecophagid monophyly. Documentation of the morphological transformations that lead to the myrmecophagid condition is hampered by incomplete data on feeding apparatus structure in nonmyrmecophagid xenarthrans (sloths and armadillos) but a tentative character mapping onto an independently derived phylogeny is offered.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

LITERATURE CITED

  • Chan, L.-K. (1995). Extrinsic lingual musculature of two pangolins (Pholidota: Manidae). J. Mammal. 76: 472–480.

    Google Scholar 

  • Cheng, H. (1986). Anatomical studies of Manis pentadactyla's tongue and structures relative to the tongue. Mem. Beij. Nat. Hist. Soc. 36: 1–9.

    Google Scholar 

  • Committee, I. A. N. (1977). Nomina Anatomica. Excerpta Medica, Amsterdam.

    Google Scholar 

  • Crompton, A. W. (1989). The evolution of mammalian mastication. In: Complex Organismal Functions: Integration and Evolution in Vertebrates, D. B. Wake and G. Roth, eds., pp. 23–40, John Wiley and Sons, Ltd., Chichester.

    Google Scholar 

  • Davis, D. D. (1961). Origin of the mammalian feeding mechanism. Am. Zool. 1: 229–234.

    Google Scholar 

  • De Jong, W. W., Leunissen, J. A. M., and Wistow, G. J. (1993). Eye lens crystallins and the phylogeny of placental orders: Evidence for a macroscelid-paenungulate clade? In: Mammal Phylogeny, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., Vol. 2: Placentals, pp. 5–12, Springer-Verlag, New York.

    Google Scholar 

  • Dingler, E. C. (1964a). Die konstructive Form der Zunge des Ameisenbären Verh. Anat. Ges. 58: 405–416.

    Google Scholar 

  • Dingler, E. C. (1964b). Vergleichende funktionell-anatomische Studien en Edentatenzungen (Dasypus sexcinctus, Smutsia temmincki, Tamandua tetradactyla und Myrmecophaga jubata). Morph. Jb. 105: 375–395.

    Google Scholar 

  • Doran, G. A., and Allbrook, D. B. (1973). The tongue and associated structures in two species of African pangolins, Manis gigantea and Manis tricuspis. J. Mammal. 54: 887–899.

    Google Scholar 

  • Duvernoy, G. L. (1830). De la langue, considérée comme organe de préhension des alimens ou recherches anatomiques sur les mouvemens de la langue dans quelques animaux, particulièrement de la classe des mammifères et de celle des reptiles. Mém. Soc. d'Hist. Nat. Strasbourg 1: 1–16.

    Google Scholar 

  • Edgeworth, F. H. (1914). On the development and morphology of the mandibular and hyoid muscles of mammals. Q. J. Microsc. Sci. 59: 573–645.

    Google Scholar 

  • Edgeworth, F. H. (1916). On the development and morphology of the pharyngeal, laryngeal and hypobranchial muscles of mammals. Q. J. Microsc. Sci. 61: 383–432.

    Google Scholar 

  • Edgeworth, F. H. (1923). On the development of the cranial muscles of Tatusia and Manis. J. Anat. Physiol. (Lond.) 57: 313–335.

    Google Scholar 

  • Edgeworth, F. H. (1931). On the development of the external ocular, masticatory, and hyoid muscles of Monotremata. Proc. Zool. Soc. London. 1931: 809–815.

    Google Scholar 

  • Edgeworth, F. H. (1935). The Cranial Muscles of Vertebrates, Cambridge University Press, Cambridge.

    Google Scholar 

  • Ehlers, E. (1894). Der Processus Xiphoideus und seine Muskulatur von Manis macrura Erxl. und Manis tricuspis Surdev. Zool. Miszellen I. Abh. Konig. Gessel. Wissen. 39: 1–34.

    Google Scholar 

  • Eisenberg, J. F. (1981). The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation, and Behavior, University of Chicago Press, Chicago.

    Google Scholar 

  • Ellsworth, A. F. (1976). The North American Opposum: An Anatomical Atlas, Robert E. Krieger, Huntington, NY.

    Google Scholar 

  • Emmons, L. H., and Feer, F. (1990). Neotropical Rainforest Mammals, University of Chicago Press, Chicago.

    Google Scholar 

  • Engelmann, G. F. (1978). The Logic of Phylogenetic Analysis and the Phylogeny of the Xenarthra, Ph.D. dissertation, Columbia University, New York.

  • Engelmann, G. F. (1985). The phylogeny of the Xenarthra. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 51–64, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Flower, W. H. (1882). On the mutual affinities of the animals comprising the order Edantata. Proc. Zool. Soc. Lond. XXV: 358–367.

    Google Scholar 

  • Gasc, J.-P. (1967). Squellete hyobranchial. In: Traité de Zoologie, Vol. 16, P.-P. Grassé, ed., pp. 550–583, Masson et Cie, Paris.

    Google Scholar 

  • Gaudin, T. J. (1995). The ear region of edentates and the phylogeny of the Tardigrada (Mammalia, Xenarthra). J. Vert. Paleont. 15: 672–705.

    Google Scholar 

  • Gaudin, T. J., Wible, J. R., Hopson, J. A., and Turnbull, W. D. (1995). Cohort Epitheria (Mammalia: Eutheria). The morphological evidence reexamined. J. Vert. Paleont. 15: 31A.

    Google Scholar 

  • Gaudin, T. J., Wible, J. R., Hopson, J. A., and Turnbull, W. D. (1996). Reexamination of the morphological evidence for the cohort Epitheria (Mammalia: Eutheria). J. Mammal. Evol. 3: 31–79.

    Google Scholar 

  • Gregory, W. K. (1910). The orders of mammals. Bull. Am. Mus. Nat. Hist. 27: 1–524.

    Google Scholar 

  • Griffiths, M. (1968). Echidnas, Pergamon Press, Oxford.

    Google Scholar 

  • Guth, C. (1961). La Région Temporale des Édentatés, Le Puy, Haute Loire.

    Google Scholar 

  • Herring, S. W. (1972). The role of canine morphology in the evolutionary divergence of pigs and peccaries. J. Mammal. 53: 500–512.

    Google Scholar 

  • Herring, S. W. (1980). Functional design of cranial muscles: comparative and physiological studies in pigs. Am. Zool. 20: 283–293.

    Google Scholar 

  • Herring, S. W. (1993). Functional morphology of mammalian mastication. Am. Zool. 33: 289–299.

    Google Scholar 

  • Hiiemae, K., and Jenkins, F. A. (1969). The anatomy and internal architecture of the muscles of mastication in Didelphis marsupialis. Postilla 140: 1–49.

    Google Scholar 

  • Hildebrand, M. (1985). Digging of quadrupeds. In: Functional Vertebrate Morphology, M. Hildebrand, D. M. Bramble, K. F. Liem, and D. B. Wake, eds., pp. 89–109, The Belknap Press of Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Hildebrand, M. (1988). Analysis of Vertebrate Structure, John Wiley and Sons, New York.

    Google Scholar 

  • Hofer, H. O. (1988). Notes on the typology of the skull of the Myrmecophagidae (Mammalia, Edentata), Morph. Jb. 134: 329–336.

    Google Scholar 

  • Honeycutt, R. L., and Adkins, R. M. (1993). Higher level systematics of eutherian mammals: An assessment of molecular characters and phylogenetic hypotheses. Annu. Rev. Ecol. Syst. 24: 279–305.

    Google Scholar 

  • Hsu, T. C. (1965). Chromosomes of two species of anteaters. Mammal. Chrom. Newsl. 15: 108.

    Google Scholar 

  • Jorge, W., Best, R. C., and Wetzel, R. M. (1985). Chromosome studies on the silky anteater Cyclopes didactylus (Myrmecophagidae, Xenarthra, Edentata). Caryologia 38: 325–330.

    Google Scholar 

  • Kühlhorn, F. (1939). Beziehungen zwischen Ernährungsweise und Bau des Kauapparates bei einigen Gürteltier und Ameisenbärenarten. Morph. Jb. 84: 55–85.

    Google Scholar 

  • Lubosch, W. (1908). Das Kiefergelenk der Edentaten und Marsupialier. Nebst Mittheilungen über die Kaumuskulatur dieser Thiere. Semons Zool. Forsch. 4: 520–555.

    Google Scholar 

  • Luckett, W. P. (1994). Suprafamilial relationships within Marsupialia: Resolution and discordance from multidisciplinary data. J. Mammal. Evol. 2: 255–283.

    Google Scholar 

  • Luschka, H. (1868a). Der obere Schnürer des menschlichen Schlundkopfes. Z. Ration. Med. 31: 363–372.

    Google Scholar 

  • Luschka, H. (1868b). Der Schlundkopf der Menschen, H. Laupp, Tübingen.

    Google Scholar 

  • McKenna, M. C. (1975). Toward a phylogenetic classification of the Mammalia. In: Phylogeny of the Primates, W. P. Luckett and F. S. Szalay, eds., pp. 21–46, Plenum Press, New York.

    Google Scholar 

  • McKenna, M. C. (1992). The alpha crystallin A chain of the eye lens and mammalian phylogeny. Ann. Zool. Fennici 28: 349–360.

    Google Scholar 

  • McKitrick, M. C. (1993). Phylogenetic constraint in evolutionary theory: Has it any explanatory power? Annu. Rev. Ecol. Syst. 24: 307–330.

    Google Scholar 

  • Miyamoto, M. M., and Goodman, M. (1986). Biomolecular systematics of eutherian mammals: phylogenetic patterns and classification. Syst. Zool. 35: 230–240.

    Google Scholar 

  • Montgomery, G. G. (1978). The Ecology of Arboreal Folivores, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Montgomery, G. G. (1985). Movements, foraging and food habits of the four extant species of neotropical vermilinguas (Mammalia: Myrmecophagidae) In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 365–377, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Naples, V. L. (1982). Cranial osteology and function in the tree sloths, Bradypus and Choloepus. Am. Mus. Nov. 2739: 1–41.

    Google Scholar 

  • Naples, V. L. (1985a). Form and function of the masticatory musculature in the tree sloths, Bradypus and Choloepus. J. Morphol. 183: 25–50.

    Google Scholar 

  • Naples, V. L. (1985b). The superficial facial musculature in sloths and vermilinguas. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 173–189, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Naples, V. L. (1986). The morphology and function of the hyoid region in the tree sloths Bradypus and Choloepus. J. Mammal. 67: 712–724.

    Google Scholar 

  • Nene, R. V. (1978). A note on the tongue muscle of the scaly anteater, Manis gigantea. J. Biol. Sci. 21: 48–49.

    Google Scholar 

  • Norman, J. E., and Ashley, M. V. (1994). Molecular systematics of the xenarthrans. American Society of Mammalogists, Washington, DC, p. 271A.

  • Novacek, M. J. (1982). Information for molecular studies from anatomical and fossil evidence on higher eutherian phylogeny. In: Macromolecular Sequences in Systematic and Evolutionary Biology, M. Goodman, ed., pp. 3–41, Plenum Press, New York.

    Google Scholar 

  • Novacek, M. J. (1993a). Patterns of diversity in the mammalian skull. In: The Skull, J. Hanken and B. K. Hall, eds., Vol. 2: Patterns of Structural and Systematic Diversity, pp. 438–531, University of Chicago Press, Chicago.

    Google Scholar 

  • Novacek, M. J. (1993b). Reflections on higher mammalian phylogenetics. J. Mammal. Evol. 1: 3–30.

    Google Scholar 

  • Novacek, M. J., and Wyss, A. R. (1986). Higher-level relationships of the Recent eutherian orders: morphological evidence. Cladistics 2: 257–287.

    Google Scholar 

  • Novacek, M. J., Wyss, A. R., and McKenna, M. C. (1988). The major groups of eutherian mammals. In: The Phylogeny and Classification of the Tetrapods, M. J. Benton, ed., Vol. 2: Mammals pp. 31–71, Clarendon Press, Oxford.

    Google Scholar 

  • Owen, R. A. (1862). On the anatomy of the great anteater (Myrmecophaga jubata, Linn.) Trans. Zool. Soc. Lond. 4: 117–140.

    Google Scholar 

  • Parker, W. K. (1884). On the structure and development of the skull in the Mammalia. Part II: Edentata. Proc. Roy. Soc. XXXVII: 78–82.

    Google Scholar 

  • Patterson, B., Segall, W., and Turnbull, W. D. (1989). The ear region in the xenarthrans (=Edentata: Mammalia) Part I. Cingulates. Fieldiana Geol. 18: 1–46.

    Google Scholar 

  • Patterson, B., Segall, W., Turnbull, W. D., and Gaudin, T. J. (1992). The ear region in Xenarthrans (=Edentata: Mammalia) Part II. Pilosa (sloths, anteaters), palaenodonts, and a miscellany. Fieldiana Geol. 24: 1–79.

    Google Scholar 

  • Pouchet, H. (1874). Mémoires sur le grand Fourmilier (Myrmecophaga jubata). Libraire de l'Académie de Médicine de Paris, Paris.

    Google Scholar 

  • Pough, H. P., Heiser, J. B., and McFarland, W. D. (1989). Vertebrate Life, Macmillan, New York.

    Google Scholar 

  • Radinsky, L. (1985). Patterns in the evolution of ungulate jaw shape. Am. Zool. 25: 303–314.

    Google Scholar 

  • Redford, K. H. (1985a). Feeding and food preference in captive and wild giant anteaters (Myrmecophaga tridactyla). J. Zool. Lond. (A) 205: 559–572.

    Google Scholar 

  • Redford, K. H. (1985b). Food habits of armadillos. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 429–437, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Redford, K. H. (1986). Dietary specialization and variation in two mammalian myrmecophages: Variation in mammalian myrmecophagy. Rev. Chil. Hist. Nat. 59: 201–208.

    Google Scholar 

  • Redford, K. H. (1987). Ants and termites as food: Patterns of mammalian myrmecophagy. In: Current Mammalogy, Vol. 1, H. H. Genoways, ed., pp. 349–399, Plenum Press, New York.

    Google Scholar 

  • Reiss, K. Z. (1997). How The Anteater Got Its Tongue: Structure and Evolution of the Feeding Apparatus in Xenarthra and Pholidota, Ph.D. dissertation, Zoology, Cornell University, Ithaca, NY.

  • Rose, K. D., and Emry, R. J. (1993). Relationships of Xenarthra, Pholidota, and fossil “edentates”: the morphological evidence. In: Mammal Phylogeny, Vol. 2: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 81–102, Springer Verlag, New York.

    Google Scholar 

  • Saban, R. (1968). Musculature de la tête. In: Traité de Zoologie, Vol. 16, P. P. Grassé, ed., pp. 229–471, Masson et Cie, Paris.

    Google Scholar 

  • Schneider, R. (1964). Der Larynx der Saugetiere. In: Handbuch der Zoologie, J. G. Helmcke, H. V. Lengerken, and D. Starck, eds., Vol. 8, pp. 1–128, deGruyter, Berlin.

    Google Scholar 

  • Shoshani, J. (1993). Hyracoidea-Tethytheria affinity based on myological data. In: Mammal Phylogeny, Vol. 2: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 235–256, Springer Verlag, New York.

    Google Scholar 

  • Sikes, S. K. (1966). The tricuspid tree pangolin, Manis tricuspis (Rafinesque). Its remarkable tongue complex. Niger. Field 31: 99–110.

    Google Scholar 

  • Simpson, G. G. (1945). A classification of the mammals. Bull. Am. Mus. Nat. Hist. 85: 1–350.

    Google Scholar 

  • Simpson, G. G. (1978). Early mammals in South America: Fact, controversy, and mystery. Proc. Am. Phil. Soc. 122: 318–328.

    Google Scholar 

  • Simpson, G. G., and Beck, W. S. (1965). Life: An Introduction to Biology, Harcourt, Brace and World, New York.

    Google Scholar 

  • Smith, K. K. (1992). The evolution of the mammalian pharynx. Zool. J. Linn. Soc. 104: 313–349.

    Google Scholar 

  • Smith, K. K. (1993). The form of the feeding apparatus in terrestrial vertebrates: Studies of adaptation and constraint. In: The Skull, Vol. 3: Functional and Evolutionary Mechanisms, B. K. Hall and J. Hanken, eds., pp. 150–196, University of Chicago Press, Chicago.

    Google Scholar 

  • Smith, K. K. (1994). Development of craniofacial musculature in Monodelphis domestica (Marsupialia, Didelphidae). J. Morphol. 222: 149–173.

    Google Scholar 

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

    Google Scholar 

  • Starck, D. (1967). Le crâne des mammifères. Traité de Zoologie, P.-P. Grassé, ed., Masson et Cie, Paris, 16: 405–549.

    Google Scholar 

  • Storch, G. (1981). Eurotamandua joresi, eim Myrmecophagidae aus dem Eozan der Grube Messel bei Darmstadt (Mammalia, Xenarthra). Sencken. leth. 61: 247–289.

    Google Scholar 

  • Storch, G., and Habersetzer, J. (1991). Rückverlagerte Choanen und akzessorische Bulla tympanica bei rezenten Vermilingua und Eurotamndua aus dem Eozän von Messel (Mammalia: Xenarthra). Z. Saugetierk. 56: 257–271.

    Google Scholar 

  • Toldt, C. (1908). Der vordere Bauch des M. digastricus mandibulae und seine Varietäten beim Menschen (ii Theil) Sitzsungsber. Kais. Akad. Wissenschaft Wien. math. nat. Klasse CXVII(iii).

  • Van Valkenburgh, B. (1988). Trophic diversity in past and present guilds of large predatory mammals. Paleobiology 14: 155–173.

    Google Scholar 

  • Wake, D. B. (1991). Homoplasy: The result of natural selection, or evidence of design limitations. Am. Nat. 138: 543–567.

    Google Scholar 

  • Walker, W. F., and Homberger, D. G. (1992). Vertebrate Dissection, Saunders College Publishing, Fort Worth.

    Google Scholar 

  • Webb, S. D. (1985). The interrelationships of tree sloths and ground sloths. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 105–112, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Wetzel, R. M. (1985). The identification and distribution of Recent Xenarthra (=Edentata) In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 5–21, Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Windle, B. C. A., and Parsons, F. G. (1899). On the myology of the Edentata. Part I. Muscles of the head, neck and forelimb. Proc. Zool. Soc. Lond. 1899: 314–339.

    Google Scholar 

  • Wineski, L. E., and English, A. W. (1989). Phenoxyethanol as a nontoxic preservative in the dissection laboratory. Acta Anat. 136: 155–158.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reiss, K.Z. Myology of the Feeding Apparatus of Myrmecophagid Anteaters (Xenarthra: Myrmecophagidae). Journal of Mammalian Evolution 4, 87–117 (1997). https://doi.org/10.1023/A:1027366129277

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1027366129277

Navigation