Skeletal indicators of locomotor adaptations in shrews

Authors

  • Neal Woodman U.S. Geological Survey, Eastern Ecological Science Center. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution.

Keywords:

Ambulatory, anatomy, aquatic, ecomorphology, fossorial, functional morphology, Soricomorpha, substrate use, terrestrial.

Abstract

The Soricidae (Mammalia: Eulypotyphla) comprises more than 450 species inhabiting a variety of habitats on five continents. As a family, shrews employ a variety of locomotor modes that incorporate ambulatory, fossorial, aquatic, and scansorial behaviors, illustrating an ability to exploit a variety of natural substrates and their associated resources. In this study, the association of skeletal morphology and three of the dominant locomotor modes in the family—ambulatory, semi-fossorial, and semi-aquatic behaviors—was investigated in up to 52 species of 12 genera representing all three subfamilies of Soricidae. From skeletal measures, 34 morphological indices were calculated, most of which have been used previously to characterize substrate use among shrews, rodents, and other mammals, and analyzed for their individual effectiveness for discriminating the three locomotory modes. To assess their effectiveness in combination, subsets of locomotor indices were analyzed using 1) mean percentile ranks, 2) the first principal component from principal components analysis, and 3) plots and classifications from discriminant function analyses. In general, the three methods effectively identified and grouped the three locomotor modes and identified smaller subsets. Additional analyses were then used to classify the locomotor behaviors of five species whose locomotor modes were unknown or ambiguous. The analyses reinforce and broaden the scope of a previously identified observation of the wide range of grades of morphological variation that may permit an equally diverse range of locomotor abilities among the Soricidae.

Author Biography

Neal Woodman, U.S. Geological Survey, Eastern Ecological Science Center. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution.

Research Zoologist

References

BENESKI, J. T., JR., AND D.W. STINSON. 1987 . Sorex palustris. Mammalian Species 296:1–6.

CAHN, A. R. 1937. The mammals of Quetico Provincial Park of Ontario. Journal of Mammalogy 18:19–30.

CHAMBERLAIN, E. B. 1929. Behavior of the least shrew. Journal of Mammalogy 10:250–251.

CHURCHFIELD, S. 1990. The Natural History of Shrews. Comstock Publishing Associates. Ithaca, U.S.A.

DAGG, A. I., AND E. E. WINDSOR. 1972. Swimming in northern terrestrial mammals. Canadian Journal of Zoology 50:117–139.

DAVIS, W. B., AND L. JOERIS. 1945. Notes on the life history of the little short-tailed shrew. Journal of Mammalogy 26:136–138.

EISENBERG, J. F. 1981. The Mammalian Radiations. The University of Chicago Press. Chicago, U.S.A.

ELISSAMBURU, A., AND L. DE SANTIS. 2011. Forelimb proportions and fossorial adaptations in the scratch-digging rodent Ctenomys (Caviomorpha). Journal of Mammalogy 92:683–689.

FISH, F. E. 1982. Function of the compressed tail of surface swimming muskrats (Ondatra zibethicus). Journal of Mammalogy 63:591–597.

FISH, F. E. 1984. Mechanics, power output and efficiency of the swimming muskrat (Ondatra zibethicus). Journal of Experimental Biology 110:183–201.

FISH, F. E. 2000. Biomechanics and energetics in aquatic and semiaquatic mammals: platypus to whale. Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches 73:683–698.

HAMMER, Ø., D. A. T. HARPER, AND P. D. RYAN. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologica Electronica 4:1–9.

HANSKI, I. 1986. Population dynamics of shrews on small islands accord with the equilibrium model. Biological Journal of the Linnean Society 28:23–36.

HILDEBRAND, M. 1985A. WALKING AND RUNNING. Pp. 38–57, in Functional Vertebrate Morphology (Hildebrand, M., D. M. Bramble, K. F. Liem, and D. B. Wake, eds.). Belknap Press, Cambridge, U.S.A.

HILDEBRAND, M. 1985b. Digging of quadrupeds. Pp. 89–109, in Functional Vertebrate Morphology (Hildebrand, M., D. M. Bramble, K. F. Liem, and D. B. Wake, eds.). Belknap Press, Cambridge, U.S.A.

HODGSON, J. R. 1986. The occurrence of small mammals in the diets of largemouth bass (Micropterus salmoides). Jack-Pine Warbler 64:39–40.

HOPKINS, S. S. B., AND E. B. DAVIS. 2009. Quantitative morphological proxies for fossoriality in small mammals. Journal of Mammalogy 90:1449–1460.

HOWELL, H. B. 1930. Aquatic mammals. Their adaptations to life in the water. Charles C. Thomas. Springfield, USA.

HE, K., ET AL. 2015. Molecular phylogeny supports repeated adaptation to burrowing within small-eared shrews, genus of Cryptotis (Eulipotyphla, Soricidae). Plos One DOI:10.1371/journal.pone.0140280 October 21.

HE, K., ET AL. 2021. Mitogenome and comprehensive phylogenetic analyses support rapid diversifications among species groups of small eared shrews genus Cryptotis (Mammalia: Eulipotyphla: Soricidae). Zoological Research 42:739–745.

HUISH, M. T., AND D. F. HOFFMEISTER. 1947. The short-tailed shrew (Blarina) as a source of food for the green sunfish. Copeia 1947:198.

HUTTERER, R. 1985. Anatomical adaptations of shrews. Mammal Review 15:43–55.

JACKSON, H. H. T. 1928. A taxonomic review of the American long-tailed shrews (genera Sorex and Microsorex). North American Fauna 51:1–238.

JUNG, T. S., ET AL. 2011. American pygmy shrew, Sorex hoyi, consumed by an arctic grayling, Thymallus arcticus. Canadian Field Naturalist 125:255–256.

KIRK E. C., P. LEMELIN, M. W. HAMRICK, D. M. BOYER, AND J. I. BLOCH. 2008. Intrinsic hand proportions of euarchontans and other mammals: Implications for the locomotor behavior of plesiadapiforms. Journal of Human Evolution 55:278–299.

LEMELIN P. 1999. Morphological correlates of substrate use in didelphid marsupials: Implications for primate origins. Journal of Zoology 247:165–175.

LISI, P. J., ET AL. 2013. Episodic predation of mammals by stream fishes in a boreal river basin. Ecology of Freshwater Fish 23:622–630

MENDES-SOARES, H., AND L. RYCHLIK. 2009. Differences in swimming and diving abilities between two sympatric species of water shrews: Neomys anomalus and Neomys fodiens (Soricidae). Journal of Ethology 27:317–325

MOORE, J. W., AND G. J. KENAGY. 2004. Consumption of shrews, Sorex spp., by Arctic grayling, Thymallus arcticus. The Canadian Field Naturalist 118:111–115.

NATIONS, J. A., ET AL. 2019. A simple skeletal measurement effectively predicts climbing behaviour in a diverse clade of small mammals. Biological Journal of the Linnean Society 128:323–336.

PETERSEN, K. E., AND T. L. YATES. 1980. Condylura cristata. Mammalian Species 129:1–4.

PINE, R. H., N. WOODMAN, AND R. M. TIMM. 2002. Rediscovery of Enders’s small-eared shrew, Cryptotis endersi (Insectivora: Soricidae), with a redescription of the species. Mammalian Biology 67:372 –377.

PRICE, M. V. 1993. A functional–morphometric analysis of forelimbs in bipedal and quadrupedal heteromyid rodents. Biological Journal of the Linnean Society 50:339–360.

REED, C. A. 1951. Locomotion and appendicular anatomy in three soricoid insectivores. American Midland Naturalist 45:513–670.

SAMUELS, J. X., AND B. VAN VALKENBURGH. 2008. Skeletal indicators of locomotor adaptations in living and extinct rodents. Journal of Morphology 269:1387–1411.

SARGIS, E. J. 2002. Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. Journal of Morphology 253:10–42.

SARGIS, E. J., ET AL. 2013a. Using hand proportions to test taxonomic boundaries within the Tupaia glis species complex (Scandentia, Tupaiidae). Journal of Mammalogy 94:183–201.

SARGIS, E. J., ET AL. 2013b. Morphological distinctiveness of Javan Tupaia hypochrysa (Scandentia, Tupaiidae). Journal of Mammalogy 94:938–947.

SHIMER, H. W. 1903. Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals. III. Fossoriality. American Naturalist 37:819–825.

SORENSON, M. W. 1962. Some aspects of water shrew behavior. American Midland Naturalist 68:445–462.

TAPISSO, J. T., ET AL. 2013. Ecological release: swimming and diving behavior of an allopatric population of the Mediterranean water shrew. Journal of Mammalogy 94:29–39.

TUTTLE, M. D. 1964. Observation of Sorex cinereus. Journal of Mammalogy 45:148.

VIZCAINO, S. F., AND N. MILNE. 2002. Structure and function in armadillo limbs (Mammalia: Xenarthra: Dasypodidae). Journal of Zoology 257:117–127.

WAHAB, M. F. A., ET AL. 2020. Taxonomic assessment of the Malayan water shrew Chimarrogale hantu Harrison, 1958 and reclassification to the genus Crossogale. Mammalian Biology 100:399–409.

WOODMAN, N. 2019. Three new species of small-eared shrews, genus Cryptotis, from El Salvador and Guatemala (Mammalia: Eulipotyphla: Soricidae). Special Publication of the Museum of Texas Tech University 72:1–46.

WOODMAN, N., AND S. A. GAFFNEY. 2014. Can they dig it? Functional morphology and degrees of semi-fossoriality among some American shrews (Mammalia, Soricidae). Journal of Morphology 275:745–759.

WOODMAN, N., AND J. P. J. MORGAN. 2005. Skeletal morphology of the forefoot in shrews (Mammalia: Soricidae) of the genus Cryptotis, as revealed by digital x-rays. Journal of Morphology 266:60–73.

WOODMAN, N., AND F. A. STABILE. 2015a. Variation in the myosoricine hand skeleton and its implications for locomotory behavior (Eulipotyphla: Soricidae). Journal of Mammalogy 96:159–171.

WOODMAN, N., AND F. A. STABILE. 2015b. Functional skeletal morphology and its implications for locomotory behavior among three genera of mysoricine shrews (Eulipotyphla: Soricidae). Journal of Morphology 276:550–563.

WOODMAN, N., AND R. B. STEPHENS. 2010. At the foot of the shrew: manus morphology distinguishes closely-related Cryptotis goodwini and Cryptotis griseoventris (Mammalia, Soricidae) in Central America. Biological Journal of the Linnean Society 99:118–134.

WOODMAN, N., AND R. M. TIMM. 2016. A new species of small-eared shrew in the Cryptotis thomasi species group from Costa Rica (Mammalia: Eulipotyphla: Soricidae). Mammal Research 62:89–101 (published online 27 August 2016).

WOODMAN, N., AND A. T. WILKEN. 2019. Comparative functional skeletal morphology among three genera of shrews: implications for the evolution of locomotory behavior in the Soricinae (Eulipotyphla: Soricidae). Journal of Mammalogy 100:1750–1764.

WOODMAN, N., A. T. WILKEN, AND S. IKRAM. 2019. See how they ran: morphological and functional aspects of skeletons from ancient Egyptian shrew mummies (Eulipotyphla: Soricidae: Crocidurinae). Journal of Mammalogy 100:1199–1210.

Downloads

Additional Files

Published

2023-01-27

Issue

Section

Special Contribution