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Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Molar crests and body mass as dietary indicators in marsupials

Aaron S. Hogue A B and Shakila ZiaShakeri A
+ Author Affiliations
- Author Affiliations

A Salisbury University, Department of Biological Sciences, 1101 Camden Avenue, Salisbury, MD 21801, USA.

B Corresponding author. Email: ashogue@salisbury.edu

Australian Journal of Zoology 58(1) 56-68 https://doi.org/10.1071/ZO09084
Submitted: 13 August 2009  Accepted: 27 February 2010   Published: 7 April 2010

Abstract

The discovery of ecomorphological relationships in mammals is important not only in its own right, but also for its potential in shedding light on the ecology of extinct and poorly known species. Two such potential relationships are the proposed connection between molar shear crests and body mass to diet. Research on primates suggests that, owing to the digestive challenges of structural carbohydrates (in foliage and insects), folivores and insectivores differ from other species in needing relatively long molar shear crests. These studies also suggest that metabolic constraints force folivores to be consistently larger than insectivores, with 500–700 g being the proposed body mass boundary between the two. This study tests these proposed ecomorphological links in a diverse sample of 64 marsupial species. As predicted, folivores and insectivores have significantly relatively longer molar shear crests than other species. Similarly, folivores are significantly larger than insectivores, as predicted, though the proposed body mass boundary was not supported. These results suggest that shear crest length and body mass are indeed linked to diet in the proposed manner. It may now be possible to use these findings to gain a greater understanding of the feeding behaviours of a variety of extinct marsupials and other therians.


Acknowledgements

We are extremely grateful to M. Ravosa, M. Dagosto, B. Shea, R. Kay, and J. Flynn for their extensive guidance in the development, completion, and publication of this research. We thank S. Stephens and L. Salas for providing data before publication. Lastly, we thank the following for allowing access to museum collections: R. Voss, C. Norris, and B. Randall (American Museum of Natural History), M. Archer, T. Ennis, and S. Ingleby (Australian Museum), P. Jenkins (British Museum of Natural History), L. Heaney, B. Patterson, and W. Stanley (Field Museum of Natural History), L. Abraczinskas and B. Lundrigan (Michigan State University Museum), L. Frigo (Museum of Victoria), L. Gordon and R. Thorington (Smithsonian Institution), T. Flannery, D. Stemmer, and C. Kemper (South Australian Museum). This research was funded by generous grants from the American Society of Mammalogists, the National Science Foundation (Grant # NSF BCS-0127915), and Sigma Xi.


References

Abbie, A. A. (1939). A masticatory adaptation peculiar to some diprotodont marsupials. Proceedings of the Zoological Society of London 109, 261–279.
Archer M. (1984). The Australian marsupial radiation. In ‘Vertebrate Zoogeography & Evolution in Australasia’. (Eds M. Archer and G. Clayton.) pp. 633–808. (Hesperian Press: Carlisle.)

Bininda-Emonds, O. R. P. , Cardillo, M. , Jones, K. E. , MacPhee, R. D. E. , Beck, R. M. D. , Grenyer, R. , Price, S. A. , Vos, R. A. , Gittleman, J. L. , and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507–512.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Cartmill M. (1972). Arboreal adaptation and the origin of the order Primates. In ‘The Functional and Evolutionary Biology of Primates’. (Ed. R. H. Tuttle.) pp. 97–122. (Aldine-Atherton: Chicago.)

Cartmill M. (1974). Daubentonia, Dactylopsila, woodpeckers and klinorhynchy. In ‘Prosimian Biology’. (Ed. A. Walker.) pp. 655–670. (Duckworth: London.)

Cheverud, J. M. , and Dow, M. M. (1985). An autocorrelation analysis of the effect of lineal fission on genetic variation among social groups. American Journal of Physical Anthropology 67, 113–121.
Crossref | GoogleScholarGoogle Scholar | Crompton A. W. , Lieberman D. E. , Owerkowicz T. , Baudinette R. V. , and Skinner J. (2008 b). Motor control of masticatory movements in the southern hairy-nosed wombat (Lasiorhinus latifrons). In ‘Primate Craniofacial Function and Biology’. (Eds C. J. Vinyard, M. J. Ravosa, and C. E. Wall.) pp. 83–111. (Springer: New York.)

Damuth J. , and MacFadden B. J. (Eds) (1990). ‘Body Size in Mammalian Paleobiology: Estimation and Biological Implications.’ (Cambridge University Press: New York.)

Dawson, T. J. , and Hulbert, A. J. (1970). Standard metabolism, body temperature, and surface areas of Australian marsupials. The American Journal of Physiology 218, 1233–1238.
CAS | PubMed | Gipps M. , and Sanson G. D. (1984). Mastication and digestion in Pseudocheirus. In ‘Possums and Gliders’. (Eds A. P. Smith and I. D. Hume.) pp. 237–246. (Surrey Beatty: Sydney.)

Gittleman, J. L. , and Kot, M. (1990). Adaptation: statistics and a null model for estimating phylogenetic effects. Systematic Zoology 39, 227–241.
Crossref | GoogleScholarGoogle Scholar | Gittleman J. L. , and Luh H. K. (1994). Phylogeny, evolutionary models and comparative methods: a simulation study. In ‘Phylogenetics and Ecology’. (Eds P. Eggleton and R. I. Vane-Wright.) pp. 103–122. (Academic Press: London.)

Grafen, A. (1989). The phylogenetic regression. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 326, 119–157.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Hladik C. M. (1978). Phenology of leaf production in rain forests of Gabon: distribution and composition of food for folivores. In ‘The Ecology of Arboreal Folivores’. (Ed. G. G. Montgomery.) pp. 51–71. (Smithsonian Institution Press: Washington, DC.)

Hogue A. S. (2004). On the relation between craniodental form and diet in mammals: marsupials as a natural experiment. Ph.D. Thesis, Northwestern University, Evanston, IL.

Hogue A. S. (2008). Mandibular corpus form and its functional significance: evidence from ecologically convergent marsupials. In ‘Primate Craniofacial Function and Biology’. (Eds C. J. Vinyard, M. J. Ravosa, and C. E. Wall.) pp. 329–356. (Springer: New York.)

Huey, R. B. , and Bennett, A. F. (1987). Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41, 1098–1115.
Crossref | GoogleScholarGoogle Scholar | Kay R. F. , and Covert H. H. (1984). Anatomy and behavior of extinct primates. In ‘Food Acquisition and Processing in Primates’. (Ed. A. Bilsborough.) pp. 467–508. (Plenum Press: New York.)

Kay R. F. , and Hylander W. L. (1978). The dental structure of mammalian folivores with special reference to primates and Phalangeroidea. In ‘Ecology of Arboreal Folivores’. (Ed. G. G. Montgomery.) pp. 173–191. (Smithsonian Institution Press: Washington, DC.)

Kay, R. F. , and Sheine, W. S. (1979). On the relationship between chitin particle size and digestibility in the primate Galago senegalensis. American Journal of Physical Anthropology 50, 301–308.
Crossref | GoogleScholarGoogle Scholar | Kleiber M. (1961). ‘The Fire of Life.’ (Wiley: New York.)

Kozlowski, J. , and Konarzewski, M. (2004). Is West, Brown and Enquist’s model of allometric scaling mathematically correct and biologically relevant? Functional Ecology 18, 283–289.
Crossref | GoogleScholarGoogle Scholar | Lucas P. W. (2004). ‘Dental Functional Morphology: How Teeth Work.’ (Cambridge University Press: Cambridge.)

Lynch, M. (1991). Methods for the analysis of comparative data in evolutionary ecology. Evolution 45, 1065–1080.
Crossref | GoogleScholarGoogle Scholar | Martins E. P. (2004). COMPARE, version 4.6. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/. Indiana University, Bloomington.

Martins, E. P. , and Garland, T. (1991). Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 45, 534–557.
Crossref | GoogleScholarGoogle Scholar | Mitchell H. H. (1964). ‘Comparative Nutrition of Man and Domestic Animals.’ (Academic Press: New York.)

Moore, S. J. , and Sanson, G. D. (1995). A comparison of the molar efficiency of two insect-eating mammals. Journal of Zoology 235, 175–192.
Parra R. (1978). Comparison of foregut and hindgut fermentation in herbivores. In ‘The Ecology of Arboreal Folivores’. (Ed. G. G. Montgomery.) pp. 205–229. (Smithsonian Institution Press: Washington, DC.)

Reig O. A. , Kirsch J. A. W. , and Marshall L. G. (1987). Systematic relationships of the living and neocenozoic American “opossum-like” marsupials (Suborder Didelphimoria), with comments on the classification of these and of the Cretaceous and Paleogene New World and European metatherians. In ‘Possums and Opossums: Studies in Evolution’. (Ed. M. Archer.) pp. 1–89. (Surrey Beatty: Sydney.)

Ridley M. (1983). ‘The Explanation of Organic Diversity: The Comparative Method and Adaptations for Mating.’ (Clarendon Press: Oxford.)

Robinson, B. W. , and Wilson, D. S. (1998). Optimal foraging, specialization, and a solution to Liem’s Paradox. American Naturalist 151, 223–235.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Ryan C. A. , and Green T. R. (1974). Proteinase inhibitors in natural plant protection. In ‘Metabolism and Regulation of Secondary Plant Products’. (Ed. E. E. Conn.) pp. 123–140. (Academic Press: New York.)

Sanson, G. D. (1980). The morphology and occlusion of the molariform cheek teeth in some Macropodinae (Marsupialia: Macropodidae). Australian Journal of Zoology 28, 341–365.
Crossref | GoogleScholarGoogle Scholar | Sanson G. D. (1989). Morphological adaptations of teeth to diets and feeding in the Macropodoidea. In ‘Kangaroos, Wallabies and Rat-Kangaroos’. (Eds G. Grigg, P. Jarman and J. Hume.) pp. 151–168. (Surrey Beatty: Sydney.)

Schmidt-Nielsen K. (1984). ‘Scaling: Why is Animal Size so Important?’ (Cambridge University Press: Cambridge.)

Sheine, W. S. , and Kay, R. F. (1977). Analysis of chewed food particle-size and its relationship to molar structure in primates Cheirogaleus medius and Galago senegalensis and insectivoran Tupaia glis. American Journal of Physical Anthropology 47, 15–20.
Crossref | GoogleScholarGoogle Scholar | Sokal R. R. , and Rohlf F. J. (1995). ‘Biometry.’ 3rd edn. (W.H. Freeman and Co.: New York.)

Southgate R. I. (1990). Habitats and diet of the greater bilby Macrotis lagotis Reid (Marsupialia: Peramelidae). In ‘Bandicoots and Bilbies’. (Ed. C. M. Kemper.) pp. 303–309. (Surrey Beatty: Sydney.)

Springer, M. S. , Kirsch, J. A. W. , Aplin, K. , and Flannery, T. (1990). DNA hybridization, cladistics, and the phylogeny of phalangerid marsupials. Journal of Molecular Evolution 30, 298–311.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Strait S. G. (1991). Dietary reconstruction in small-bodied fossil primates. PhD Thesis, State University of New York, Stony Brook, NY.

Strait, S. G. (1993a). Differences in occlusal morphology and molar size in frugivores and faunivores. Journal of Human Evolution 25, 471–484.
Crossref | GoogleScholarGoogle Scholar | Tyndale-Biscoe H. (2005). ‘Life of Marsupials.’ (CSIRO Publishing: Melbourne.)

Van Soest, P. J. (1966). Nonnutritive residues: a system of analysis for the replacement of crude fiber. Journal – Association of Official Analytical Chemists 49, 546–557.
CAS | Vaughan T. A. , Ryan J. M. , and Czaplewski N. J. (2000). ‘Mammalogy.’ 4th edn. (Brooks Cole: Boston.)

Walker P. , and Murray P. (1975). An assessment of masticatory efficiency in a series of anthropoid primates with special reference to the Colobinae and Cercopithecinae. In ‘Primate Functional Morphology and Evolution’. (Ed. R. Tuttle.) pp. 135–150. (Aldine: New York.)

Warner, A. C. I. (1981). Rate of passage of digesta through the gut of mammals and birds. Nutrition Abstracts and Reviews 51B, 789–820.
Williams R. T. (1969). ‘Detoxification Mechanisms.’ (Wiley: New York.)

Wilson D. E. , and Reeder D. M. (Eds) (2005). ‘Mammal Species of the World. A Taxonomic and Geographic Reference.’ 3rd edn. (Johns Hopkins University Press: Baltimore.)

Yamashita N. (1996). The relationship between tooth morphology and mechanical dietary properties in two Malagasy lemur families (Lemuridae and Indriidae). Ph.D. Thesis, Northwestern University, Evanston, IL.

Yamashita, N. (1998). Functional dental correlates of food properties in five Malagasy lemur species. American Journal of Physical Anthropology 106, 169–188.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |