Pedal grasping in the northern smooth-tailed treeshrew Dendrogale murina (Tupaiidae, Scandentia): insights for euarchontan pedal evolution
Abstract
Pedal grasping evolution in euarchontan mammals is of great importance as it bears on the adaptive significance of specialized hallucal grasping and arboreal niche use related to the group differentiation. Basally divergent arboreal tupaiid treeshrews are very suitable for testing pedal grasping modes and associated substrate correlates and provide insights on euarchontan pedal evolution. For these purposes we filmed wild-caught Dendrogale murina from Vietnam and analyzed their foot mechanisms. Our observations showed that hallucal grasp was moderately used and was mainly associated with small and horizontal substrates. Convergent grasp was frequently used on medium-sized and horizontal substrates whereas claws were related to large and vertical substrates. In addition, the foot was frequently inverted and mainly placed in a semiplantigrade position. Inversion and semiplantigrady dominated on small, medium-sized and horizontal substrates but decreased on larger substrates with increased inclinations. The observed pedal mechanism probably represents a derived condition, where hallucal grasping tends to become slightly restrained, compared to the primitive euarchontan (and scandentian) pedal grasping mechanism. Furthermore, it hallmarks an early stage in tupaiid evolution towards a more constrained pedal grasping. This further substantiates pedal grasping plasticity within euarchontan mammals and highlights the strong relation between a hallucal grasping mechanism and the frequent and primary use of small slender substrates.
Acknowledgments
The authors wish to thank for the financial support provided by the Aristotle University of Thessaloniki and Lomonossov Moscow State University exchange program. Invaluable help and support to the arrangement of the experimental settings and filming were provided by E. Yakhontov and Profs. L.P. Korzoun and A.N. Kuznetsov. The current study was financially supported by Russian Science Foundation (RNF) (projects no. 14-50-00029 “Scientific Basis of the National Biobank – depository of the living systems”) and Russian Foundation for Basic Research (projects no. 15-04-05049A). We are particularly grateful to Prof. E.J. Sargis for constructive comments on earlier versions of this work. Many thanks also go to the reviewers and the editor for their suggestions that greatly improved this paper.
References
Butler, P.M. 1980. The tupaiid dentition. In: (W.P. Luckett, ed.) Comparative biology and evolutionary relationships of tree Shrews. Plenum Press, New York. pp. 171–204.10.1007/978-1-4684-1051-8_5Search in Google Scholar
Bloch, J.I. and D.M. Boyer. 2002. Grasping primate origins. Science 298: 1606–1610.10.1126/science.1078249Search in Google Scholar
Bloch, J.I. and D.M. Boyer. 2007. New skeletons of Paleocene-Eocene Plesiadapiformes: a diversity of arboreal positional behaviors in early primates. In: (M.J. Ravosa and M. Dagosto, eds.) Primate origins: adaptations and evolution. Springer, New York. pp. 535–581.10.1007/978-0-387-33507-0_16Search in Google Scholar
Bloch, J.I., M.T. Silcox, D.M. Boyer and E.J. Sargis. 2007. New Paleocene skeletons and the relationship of plesiadapiforms to crown-dlace primates. Proc. Natl. Acad. Sci. 104: 1159–1164.10.1073/pnas.0610579104Search in Google Scholar
Boyer, D.M., B.A. Patel, S.G. Larson and J.T. Stern. 2007. Telemetered electromyography of peroneus longus in Varecia variegata and Eulemur rubriventer: implications for the functional significance of a large peroneal process. J. Hum. Evol. 53: 119–134.10.1016/j.jhevol.2006.10.007Search in Google Scholar
Byron, C.D., A. Herrel, E. Pauwels, A. de Muynck and B.A. Patel. 2015. Mouse hallucal metatarsal corss-sectional geometry in a simulated fine branch niche. J. Morph. 276: 759–765.10.1002/jmor.20376Search in Google Scholar
Cartmill, M. 1972. Arboreal adaptations and the origin of the order Primates. In: (R.H. Tuttle, ed.) The functional and evolutionary biology of primates. Aldine-Atherton, Chicago. pp. 3–35.Search in Google Scholar
Cartmill, M. 1974. Pads and claws in arboreal locomotion. In: (F.A. Jenkins, Jr., ed.) Primate locomotion. Academic Press, New York. pp. 45–83.Search in Google Scholar
Davis, D.D. 1938. Notes on the anatomy of the treeshrew Dendrogale. Publ. Field Mus. Nat. Hist. Zool. Ser. 20: 384–404.10.5962/bhl.title.3056Search in Google Scholar
Emmons, L.H. 2000. Tupai. A field study of Bornean Treeshrews. University of California Press, Berkeley.10.1525/california/9780520222915.001.0001Search in Google Scholar
Endo, H., W. Rerkamuaychoke, J. Kimura, M. Sasaki, M. Kurohmaru and J. Yamada. 1999. Functional morphology of the locomotor system in the Northern Smooth-tailed Tree shrew (Dendrogale murina). Annals Anat. 181: 397–402.10.1016/S0940-9602(99)80137-XSearch in Google Scholar
Gebo, D.L. 1993. Functional morphology of the foot in primates. In: (D.L. Gebo, ed.) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, Dekalb. pp. 175–196.Search in Google Scholar
Gebo, D.L. 2004. A shrew-sized origin for primates. Yearbk. Phys. Anthropol. 47: 40–62.10.1002/ajpa.20154Search in Google Scholar PubMed
Godinot, M. 2007. Primate origins: a reappraisal of historical data favoring tupaiid affinities. In: (M.J. Ravosa and M. Dagosto, eds.) Primate origins: adaptations and evolution. Springer, New York. pp. 83–142.10.1007/978-0-387-33507-0_4Search in Google Scholar
Jenkins, F.A., Jr. 1974. Tree shrew locomotion and the origins of primate arborealism. In: (F.A. Jenkins, Jr., ed.) Primate locomotion. Academic Press, New York. pp. 85–116.Search in Google Scholar
Jenkins, F.A., Jr. and D. McClearn. 1984. Mechanisms of hind foot reversal in climbing mammals. J. Morph. 182: 197–219.10.1002/jmor.1051820207Search in Google Scholar PubMed
Kloss, C.B. 1916. On a collection of mammals from the coast and islands of South-east Siam. Proc. Zool. Soc. Lond. 1916: 27–75.10.1111/j.1096-3642.1916.tb02008.xSearch in Google Scholar
Kvartalnov, P.V. 2009. Ecology and behavior of the slender-tailed tree-shrew (Dendrogale murina, Scandentia). Zool. Zhurnal 88: 1387–1395. [in Russian with English summary].10.1134/S1062359022070093Search in Google Scholar
Le Gros Clark, W.E. 1926. On the anatomy of the pen-tailed tree shrew (Ptilocercus lowii). Proc. Zool. Soc. Lond. 1926: 1179–1309.10.1111/j.1096-3642.1926.tb02241.xSearch in Google Scholar
Le Gros Clark, W.E. 1959. The Antecedents of Man. Edinburgh University Press, Edinburgh. pp. 374.Search in Google Scholar
Lekagul, B. and J.A. McNeely. 1977. Mammals of Thailand. Association for the Conservation of Wildlife, Bangkok. pp. 758.Search in Google Scholar
Luckett, W.P. 1980. The suggested evolutionary relationships and classification of tree shrews. In: (W.P. Luckett, ed.) Comparative biology and evolutionary relationships of Tree Shrews. Plenum Press, New York. pp. 3–31.10.1007/978-1-4684-1051-8_1Search in Google Scholar
Martin, R.D. 1990. Primate origins and evolution. Princeton University Press, Princeton. pp. 840.Search in Google Scholar
Martin, P. and P. Bateson. 1993. Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge. pp. 222.10.1017/CBO9781139168342Search in Google Scholar
O’Leary, M.A., J.I. Bloch, J.J. Flynn, T.J. Gaudin, A. Giallombardo, N.P. Giannini, S.L. Goldberg, B.P. Kraatz, Z.-X. Luo, J. Meng, X. Ni, M.J. Novacek, F.A. Perini, Z. Randall, G.W. Rougier, E.J. Sargis, M.T. Silcox, N.B. Simmons, M. Spaulding, P.M. Velazco, M. Weksler, J.R. Wible and A.L. Cirranello. 2013. The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339: 662–667.10.1126/science.1229237Search in Google Scholar PubMed
Olson, L.E., E.J. Sargis and R.D. Martin. 2004. Phylogenetic relationships among treeshrews (Scandentia): a review and critique of the morphological evidence. J. Mammal. Evol. 11: 49–71.10.1023/B:JOMM.0000029145.28207.6dSearch in Google Scholar
Olson, L.E., E.J. Sargis and R.D. Martin. 2005. Intraordinal phylogenetics of treeshrews (Mammalia: Scandentia) based on evidence from the mitochondrial 12S rRNA gene. Mol. Phyl. Evol. 35: 656–673.10.1016/j.ympev.2005.01.005Search in Google Scholar PubMed
Patel, B.A., S.G. Larson and J.T. Stern, Jr., 2015. Electromyography of crural and pedal muscles in tufted capuchin monkeys (Sapajus apella): Implications for hallucal grasping behavior and first metatarsal morphology in Euprimates. Am. J. Phys. Anthrop. 156: 553–564.10.1002/ajpa.22723Search in Google Scholar PubMed
Riesenfeld, A. 1974. Metatarsal robusticity in primates and a few other plantigrade mammals. Primates 15: 1–25.10.1007/BF01749589Search in Google Scholar
Roberts, T.E., H.C. Lanier, E.J. Sargis and L.E. Olson. 2011. Molecular phylogeny of treeshrews (Mammalia: Scandentia) and the timescale of diversification in Southeast Asia. Mol. Phyl. Evol. 60: 358–372.10.1016/j.ympev.2011.04.021Search in Google Scholar
Sargis, E.J. 2001. The grasping behaviour, locomotion and substrate use of the tree shrews Tupaia minor and T. tana (Mammalia, Scandentia). J. Zool. 253: 485–490.10.1017/S0952836901000449Search in Google Scholar
Sargis, E.J. 2002a. Functional morphology of the hindlimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J. Morphol. 254: 148–185.10.1002/jmor.10025Search in Google Scholar
Sargis, E.J. 2002b. A multivariate analysis of the postcranium of tree shrews (Scandentia, Tupaiidae) and its taxonomic implications. Mammalia 66: 579–598.10.1515/mamm.2002.66.4.579Search in Google Scholar
Sargis, E.J. 2002c. The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae): an Analysis of primatomorphan and volitantian characters. J. Mammal. Evol. 9: 137–160.10.1023/A:1021387928854Search in Google Scholar
Sargis, E.J. 2002d. Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J. Morph. 253: 10–42.10.1002/jmor.1110Search in Google Scholar
Sargis, E.J. 2007. The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae) and its implications for primate supraordinal relationships. In: (M.J. Ravosa and M. Dagosto, eds.) Primate origins: adaptations and evolution. Springer, New York. pp. 51–82.10.1007/978-0-387-33507-0_3Search in Google Scholar
Sargis, E.J., D.M. Boyer, J.I. Bloch and M.T. Silcox. 2007. Evolution of pedal grasping in primates. J. Hum. Evol. 53: 103–107.10.1016/j.jhevol.2007.01.008Search in Google Scholar
Schilling, N. and M.S. Fischer. 1999. Kinematic analysis of treadmill locomotion of tree shrews, Tupaia glis (Scandentia: Tupaiidae). Z. Saugetierk. 64: 129–153.Search in Google Scholar
Stafford, B.J. and R.W. Thorington, Jr. 1998. Carpal development and morphology in archontan mammals. J. Morph. 235: 135–155.10.1002/(SICI)1097-4687(199802)235:2<135::AID-JMOR4>3.0.CO;2-8Search in Google Scholar
Sussman, R.W. 1991. Primate origins and the evolution of angiosperms. Am. J. Primatol. 23: 209–223.10.1002/ajp.1350230402Search in Google Scholar
Szalay, F.S. and M. Dagosto. 1988. Evolution of hallucial grasping in the primates. J. Hum. Evol. 17: 1–33.10.1016/0047-2484(88)90047-4Search in Google Scholar
Szalay, F.S. and G. Drawhorn. 1980. Evolution and diversification of the Archonta in an arboreal milieu. In: (W.P. Luckett, ed.) Comparative biology and evolutionary relationships of tree shrews. Plenum Press, New York. pp. 133–169.10.1007/978-1-4684-1051-8_4Search in Google Scholar
Szalay, F.S. and S.G. Lucas. 1996. The postcranial morphology of Paleocene Chriacus and Mixodectes and the phylogenetic relationships of archontan mammals. Bull. New Mex. Mus. Nat. Hist. Sci. 7: 1–47.Search in Google Scholar
Timmins, R.J., J.W. Duckworth, C.R. Robson and J.L. Walston. 2003. Distribution, status and ecology of the mainland slender-tailed treeshrew Dendrogale murina. Mammal Rev. 33: 272–283.10.1046/j.1365-2907.2003.00013.xSearch in Google Scholar
Urbani, B. and D. Youlatos. 2013. Positional behavior and substrate use of Micromys minutus (Rodentia: Muridae): insights for understanding primate origins. J. Hum. Evol. 64: 130–136.10.1016/j.jhevol.2012.10.006Search in Google Scholar PubMed
Youlatos, D. and A. Samaras. 2011. Arboreal locomotor and postural behaviour of European red squirrels (Sciurus vulgaris L.) in northern Greece. J. Ethol. 29: 235–242.10.1007/s10164-010-0248-7Search in Google Scholar
Youlatos, D., N.E. Karantanis, C.D. Byron and A. Panyutina. 2015. Pedal grasping in an arboreal rodent relates to above-branch behavior on slender substrates. J. Zool. 296: 239–248.10.1111/jzo.12237Search in Google Scholar
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Articles in the same Issue
- Frontmatter
- Original Studies
- Exploring the potential of brown bear (Ursus arctos arctos) as a long-distance seed disperser: a pilot study in South-Western Europe
- Daily activity pattern of reintroduced giant anteaters (Myrmecophaga tridactyla): effects of seasonality and experience
- Body temperature and microhabitat use in the hibernating Japanese dormouse (Glirulus japonicus)
- Richness, diversity and abundance of bats from a savanna landscape in central Brazil
- New records of bat species using Gatkop Cave in the maternal season
- Changes of bat species composition over altitudinal gradients on northern and southern aspects of the Soutpansberg mountain range, South Africa
- Pedal grasping in the northern smooth-tailed treeshrew Dendrogale murina (Tupaiidae, Scandentia): insights for euarchontan pedal evolution
- Phylogenetic position of a monotypic Ethiopian endemic rodent genus Megadendromus (Rodentia, Nesomyidae)
- Methodology for the estimation of the age categories of Hydrochoerus hydrochaeris (Rodentia, Hydrochoeridae) through the cranial and femur morphometry
- Short Notes
- Evidence for naturalization of the American mink (Neovison vison) in Friuli Venezia Giulia, NE Italy
- Activity, movement, home range and habitat use of an adult gray wolf in a Mediterranean landscape of northern Greece
- Landscape attributes determine bobcat (Lynx rufus escuinapae) presence in Central Mexico
- Fruit selection of a binturong (Arctictis binturong) by focal animal sampling in Sabah, Malaysian Borneo
- Gross anatomy of the stomach and intestine of an Antarctic minke whale (Balaenoptera bonaerensis)
- Recent observation for leopard Panthera pardus in Egypt
Articles in the same Issue
- Frontmatter
- Original Studies
- Exploring the potential of brown bear (Ursus arctos arctos) as a long-distance seed disperser: a pilot study in South-Western Europe
- Daily activity pattern of reintroduced giant anteaters (Myrmecophaga tridactyla): effects of seasonality and experience
- Body temperature and microhabitat use in the hibernating Japanese dormouse (Glirulus japonicus)
- Richness, diversity and abundance of bats from a savanna landscape in central Brazil
- New records of bat species using Gatkop Cave in the maternal season
- Changes of bat species composition over altitudinal gradients on northern and southern aspects of the Soutpansberg mountain range, South Africa
- Pedal grasping in the northern smooth-tailed treeshrew Dendrogale murina (Tupaiidae, Scandentia): insights for euarchontan pedal evolution
- Phylogenetic position of a monotypic Ethiopian endemic rodent genus Megadendromus (Rodentia, Nesomyidae)
- Methodology for the estimation of the age categories of Hydrochoerus hydrochaeris (Rodentia, Hydrochoeridae) through the cranial and femur morphometry
- Short Notes
- Evidence for naturalization of the American mink (Neovison vison) in Friuli Venezia Giulia, NE Italy
- Activity, movement, home range and habitat use of an adult gray wolf in a Mediterranean landscape of northern Greece
- Landscape attributes determine bobcat (Lynx rufus escuinapae) presence in Central Mexico
- Fruit selection of a binturong (Arctictis binturong) by focal animal sampling in Sabah, Malaysian Borneo
- Gross anatomy of the stomach and intestine of an Antarctic minke whale (Balaenoptera bonaerensis)
- Recent observation for leopard Panthera pardus in Egypt