Digestive system of the Laotian rock rat Laonastes aenigmamus (Rodentia: Diatomyidae) from the evolutionary viewpoint

A.E. Scopin, A.P. Saveljev, N.A. Suntsova, S. Gnophanxay, A.N. Tikhonov and A.V. Abramov

Proceedings of the Zoological Institute RAS, 2011, 315(1): 3–18   ·   https://doi.org/10.31610/trudyzin/2011.315.1.3

Full text  

Abstract

A preliminary study of the gastrointestinal tract of Laonastes aenigmamus Jenkins et al., 2005 has been carried out. We have revealed that Laonastes is the smallest folivorous mammal with the enlarged forestomach, which is similar to that of certain herbivorous marsupials. The stomach of this rodent contains 70% of the digesta and performs the main role in storing and digesting of plant foods. Laonastes is a unique rodent having such the digestive system, and its herbivory is confirmed by the enlarged ampulla duodeni, small dimensions of the hindstomach (pars pylorica), the absence of vesica fellea, the presence of colon spiral loops, the well-developed lymphoid tissue of stomach, and the gut mass making up to 25–27% of the entire body mass. Such the gastrointestinal tract might have evolved as a result of a general digestive strategy of the foregut mammals that inhabited tropical forests in the Miocene. This strategy involved an adaptation to the nutrition on leaves of tropical dycots which apparently contributed to the convergent evolution of the digestive system in different folivorous mammals.

Key words

Laonastes, rodents, stomach, digestive system, foregut, folivory, evolution

Submitted August 1, 2010  ·  Accepted January 20, 2011  ·  Published March 30, 2011

References

Agadjanian A.K. 2009. Micromammalia of the Russian Plain in the Pliocene-Pleistocene. Proceedings of the Paleontological Institute of the Russian Academy of Science (Moscow), 289: 1–676. [In Russian].

Alexander R.M. 2003. A rodent as big as a buffalo. Science, 301: 1678–1679. https://doi.org/10.1126/science.1090964

Agusti J. and Anton M. 2002. Mammoths, Sablertooths, and Hominids: 65 Million Years of Mammalian Evolution in Europe. Columbia University Press, New York, 313 p.

Arendt J. and Reznick D. 2008. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends in Ecology and Evolution, 23: 26–32. https://doi.org/10.1016/j.tree.2007.09.011

Barboza P.S., Parker K.L. and Hume I.D. 2009. Integrative Wildlife Nutrition. Springer Verlag, Berlin and Heidelberg, 342 p. https://doi.org/10.1007/978-3-540-87885-8

Baskin J.A. 1996. Systematic revision of Ctenodactylidae (Mammalia, Rodentia) from the Miocene of Pakistan. Palaeovertebrata, 25: 1–49.

Bauchop T. and Martucci R.W. 1968. Ruminant-like digestion of the langur monkey. Science, 161: 698–700. https://doi.org/10.1126/science.161.3842.698

Behmann H. 1973. Vergleichend- und funktionell-anatomische Untersuchungen am Caecum und Colon myomorpher Nagetiere. Zeitschrift für Wissenschaftliche Zoologie, 186: 173–294.

Beintema J.J., Rodewald K., Braunitzer G., Czelusniak J. and Goodman M. 1991. Studies on the phylogenetic position of the Ctenodactylidae (Rodentia). Molecular Biology and Evolution, 8: 151–154.

Benefit B.R. 2000. Old World monkey origins and diversification: an evolutionary study of diet and dentition. In: P.F. Whitehead and C.J. Jolly (Eds.). Old World Monkeys. Cambridge University Press, Cambridge: 133–179. https://doi.org/10.1017/CBO9780511542589.007

Berry R.J. 1996. Small mammal differentiation on islands. Phylosophical Transactions of the Royal Society London, ser. B, 351: 753–764. https://doi.org/10.1098/rstb.1996.0070

Bodmer R. and Ward D. 2006. Frugivory in large mammalian herbivores. In: K. Danell, P. Duncan, R. Bergstrom and J. Pastor (Eds.). Large Herbivory Ecology, Ecosystem, Dynamics and Conservation. Cambridge University Press, Cambridge: 232–260. https://doi.org/10.1017/CBO9780511617461.010

Bradley S.R. and Deavers D.R. 1980. A re-examination of the relationship between thermal conductance and body weight in mammals. Comparative Biochemistry and Physiology, Part A, 65: 465–476. https://doi.org/10.1016/0300-9629(80)90060-2

Brown J.H. and Sibley R.M. 2006. Life-history evolution under a production constraint. Proceedings of the National Academy of Sciences, U.S.A., 103: 17595–17599. https://doi.org/10.1073/pnas.0608522103

Carleton M. 1973. A survey of gross stomach morphology in New World Cricetinae (Rodentia, Muroidea), with comments on functional interpretations. Miscellaneous Publications of Museum of Zoology, University of Michigan, 146: 1–43.

Caton J.M. 1999. Digestive strategy of the Asian colobine genus Trachypithecus. Primates, 40: 311–325. https://doi.org/10.1007/BF02557555

Chapman C.A. and Chapman L.J. 1991. The foraging itinerary of spider monkey: when to eat leaves? Folia Primatologica, 56: 162–166. https://doi.org/10.1159/000156542

Cerling T.E., Harris J.M., MacFadden B.J., Leakey M.G., Quade J., Eisenmann V. and Ehleringer J.R. 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature, 389: 153–158. https://doi.org/10.1038/38229

Chivers D.J. 1989. Adaptations of digestive systems in non-ruminant herbivores. Proceedings of the Nutrition Society, 48: 59–67. https://doi.org/10.1079/PNS19890010

Chivers D.J. and Hladick C.M. 1980. Morphology of gastrointestinal tract in Primates: comparisons with other mammals in relation to diet. Journal of Morphology, 166: 337–386. https://doi.org/10.1002/jmor.1051660306

Claridge A., Seebeck J. and Rose R. 2007. Bettongs, Potoroos, and the Musky Rat-Kangaroo. CSIRO Publ., Collingwood, 182 p. https://doi.org/10.1071/9780643095083

Clauss M., Frey R., Kiefer B., Lechner-Doll M., Loehlein W., Polster C., Rossner G.E. and Streich W.J. 2003. The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia, 136: 14–27. https://doi.org/10.1007/s00442-003-1254-z

Clements R., Sodhi N.S., Schilthuizen M. and Ng P.K.L. 2006. Limestone karsts of Southeast Asia: imperiled arks of biodiversity. BioScience, 56: 733–742. https://doi.org/10.1641/0006-3568(2006)56[733:LKOSAI]2.0.CO;2

Clutton-Brock T.H. and Harvey P.H. 1983. The functional significance of variation in body size among mammals. Special Publication of the American Society of Mammalogy, 7: 632–663.

Collinson M.E. and Hooker J.J. 1991. Fossil evidence of interactions between plants and plant-eating mammals. Phylosophical Transactions of the Royal Society. London, ser. B, 333: 197–208. https://doi.org/10.1098/rstb.1991.0068

Cork S.J. 1994. Digestive constraints on dietary scope in small and moderately-small mammals: how much do we really understand? In: D.J. Chivers and P. Langer (Eds.). The Digestive System in Mammals: Food, Form and Function. Cambridge University Press, Cambridge: 337–369. https://doi.org/10.1017/CBO9780511661716.022

Cork S.J. and Foley W.J. 1991. Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defenses in temperate and tropical forests. In: R.T. Palo and Ch.T. Robbins (Eds.). Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton: 133–166.

Dawson M.R., Marivaux L., Li C.K., Beard K.C. and Metais G. 2006. Laonastes and the “Lazarus effect” in recent mammals. Science, 311: 1456–1458. https://doi.org/10.1126/science.1124187

De Barros Moraes P.T., Pacheco M.R., de Souza W.M., da Silva R.A., Neto P.B.S., de Figueiredo Barreto C.S. and Ribeiro A.A.C.M. 2002. Morphological aspects of the capybara stomach (Hydrochaeris hydrochaeris): gross and microscopic structure. Anatomy, Histology, Embryology, 31: 362–366. https://doi.org/10.1046/j.1439-0264.2002.00418.x

Dutton J.F. and Barron E.J. 1997. Miocene to present vegetation changes: A possible piece of the Cenozoic cooling puzzle. Geology, 25: 39–41. https://doi.org/10.1130/0091-7613(1997)025<0039:MTPVCA>2.3.CO;2

Edwards E.J., Osborne C.P., Stromberg C.A.E., Smith S.A. and C4 Grass Consortium. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science, 328: 587–591. https://doi.org/10.1126/science.1177216

Fisher D.C. 1990. Rates of evolution – living fossils. In: D. E.G. Briggs and P.R. Crowther (Eds.). Palaeobiology: a Synthesis. Blackwell Science Ltd., Oxford: 152–159.

Fleagle J.G. 1988. Primate Adaptation and Evolution. Academic Press, San Diego, New York et al., 486 p. https://doi.org/10.1016/B978-0-12-260340-2.50012-2

Flynn L.J. 2007. Origin and evolution of the Diatomyidae, with clues to paleoecology from the fossil record. Bulletin of Carnegie Museum of Natural History, 39: 173–181. https://doi.org/10.2992/0145-9058(2007)39[173:OAEOTD]2.0.CO;2

Foley W.J. and Cork S.J. 1992. Use of fibrous diets by small herbivores: how far can the rules be “bent”? Trends of Ecology and Evolution, 7(5): 159–162. https://doi.org/10.1016/0169-5347(92)90210-3

Gilyarov M.S. 1985. On “living fossils”. Zhurnal Obshchei Biologii, 46: 190–200. [In Russian].

Gorgas M. 1967. Vergleichend-anatomische Untersuchungen am Magen-Darm-Kanal der Sciuromorpha, Hystricomorpha und Caviomorpha (Rodentia). Zeitschrift für Wissenschaftliche Zoologie, 175: 237–404.

Graur D., Hide W.A. and Li W.H. 1991. Is the guinea-pig a rodent? Nature, 351: 649–652. https://doi.org/10.1038/351649a0

Graur D., Hide W.A., Zharkikh A. and Li W.H. 1992. The biochemical phylogeny of guinea-pig and gundis, and the paraphyly of the order Rodentia. Comparative Biochemistry and Physiology. Pt.B, 101: 495–498. https://doi.org/10.1016/0305-0491(92)90327-N

Hautier L. and Saksiri S. 2009. Masticatory muscle architecture in the Laotian rock rat Laonastes aenigmamus (Mammalia, Rodentia): new insights into the evolution of hystricognathy. Journal of Anatomy, 215: 401–410. https://doi.org/10.1111/j.1469-7580.2009.01130.x

Hayssen V. 2009. Bradypus tridactylus (Pilosa: Bradypodidae). Mammalian Species, 41(839): 1–9. https://doi.org/10.1644/839.1

Hayssen V. 2010. Bradypus variegatus (Pilosa: Bradypodidae). Mammalian Species, 42(850): 19–32. https://doi.org/10.1644/850.1

Hill W.C.O. and Rewell R.E. 1948. The caecum of Primates. Transactions of the Zoological Society of London, 26: 199–246. https://doi.org/10.1111/j.1096-3642.1948.tb00223.x

Hill W.C.O. and Rewell R.E. 1954. The caecum of monotremes and marsupials. Transactions of the Zoological Society of London, 28: 185–224. https://doi.org/10.1111/j.1096-3642.1954.tb00234.x

Hohmann G. 2009. The diets of non-human primates: frugivory, food processing, and food sharing. In: J.-J. Hublin and M.P. Richards (Eds.).The Evolution of Hominin Diets: Integrating Approaches to the Study of Palaeolithic Subsistence. Springer-Verlag, Berlin and Heidelberg: 1–14. https://doi.org/10.1007/978-1-4020-9699-0_1

Honeycutt R.L. 2009. Rodents (Rodentia). In: S.B. Hedges and S. Kumar (Eds.). The Timetree of Life. Oxford University Press, Oxford: 490–494.

Huchon D. E., Chevret P., Jordan U., Kilpatrick C.W., Ranwez V., Jenkins P.D., Brosius J. and Schmitz J. 2007. Multiple molecular evidences for a living mammalian fossil. Proceedings of the National Academy of Sciences, U.S.A., 104: 7495–7499. https://doi.org/10.1073/pnas.0701289104

Hume I.D. 1999. Marsupial Nutrition. Cambridge University Press, Cambridge, 434 p.

Hume I.D. 2006. Nutrition and digestion. In: P.J. Armati, Ch.R. Dickman and I.D. Hume (Eds.). Marsupials. Cambridge Univ. Press, Cambridge et al.: 137–158. https://doi.org/10.1017/CBO9780511541889.006

Hume I.D., Jarman P.J., Renfree M.B. and Temple-Smith P.D. 1989. Macropodidae. In: D.W. Walton and B.J. Richardson (Eds.). Fauna of Australia. Australian Government Publishing Service, Canberra, 1B: 679–715.

Hume I.D., Jazwinski E. and Flannery T.F. 1993. Morphology and function of the digestive tract in New Guinean possums. Australian Journal of Zoology, 41: 85–100. https://doi.org/10.1071/ZO9930085

Iason G.R. and Villalba J.J. 2006. Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance-tolerance continuum. Journal of Chemical Ecology, 32: 1115–1132. https://doi.org/10.1007/s10886-006-9075-2

Jacobs B.F., Kingston J.D. and Jacobs L.L. 1999. The origin the grass-dominated ecosystems. Annals of the Missouri Botanical Garden, 86: 590–643. https://doi.org/10.2307/2666186

Janis Ch.M. 1989. A climatic explanation for patterns of evolutionary diversity in ungulate mammals. Paleontology, 32: 463–481.

Janis Ch.M. 1993. Tertiary mammal evolution in the context of changing climated vegetation and tectonic events. Annual Review of Ecology and Systematics, 24: 467–500. https://doi.org/10.1146/annurev.es.24.110193.002343

Janis Ch.M. 2000. Patterns in the evolution of herbivory in large terrestrial mammals: the Paleogene of North America. In: H.-D. Sues (Ed.). Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the Fossil Record. Cambridge Univ. Press, Cambridge: 168–222. https://doi.org/10.1017/CBO9780511549717.008

Janis Ch.M. 2008. An evolutionary history of browsing and grazing ungulates. In: I.J. Gordon and H.H.T. Prins (Eds.). The Ecology of Browsing and Grazing. Springer-Verlag, Berlin and Heidelberg: 21–45. https://doi.org/10.1007/978-3-540-72422-3_2

Janis Ch.M., Damuth J. and Theodor J.M. 2004. The species richness of Miocene browsers, and implications for habitat type and primary productivity in the North American grassland biome. Palaeogeography, Palaeoclimatology, Palaeoecology, 207: 371–398. https://doi.org/10.1016/j.palaeo.2003.09.032

Jenkins P.D., Kilpatrick C.W., Robinson M.F. and Timmins R.J. 2005. Morphological and molecular investigations of a new family, genus and species of rodent (Mammalia: Rodentia: Hystricognatha) from Lao PDR. Systematics and Biodiversity, 2: 419–454. https://doi.org/10.1017/S1477200004001549

Jenkins P.D. and Robinson M.F. 2002. Another variation on the gymnure theme: description of a new species of Hylomys (Lipotyphla, Erinaceidae, Galericinae). Bulletin of the Natural History Museum: Zoology Ser., London, 68: 1–11. https://doi.org/10.1017/S0968047002000018

Karasov W.H. and Martinez del Rio C. 2007. Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins. Princeton University Press, Princeton-Oxford, 741 p. https://doi.org/10.1515/9780691213316

Kay R.F. 1984. On the use of anatomical features to infer foraging behavior in extinct primates. In: P.S. Rodman and J.G. Cant (Eds.). Adaptation for Foraging in Nonhuman Primates. Columbia University Press, New York: 21–53. https://doi.org/10.7312/rodm90184-003

Kay R.N.B. and Davies A.G. 1994. Digestive physiology. In: A.G. Davies and J.F. Oates (Eds.). Colobine Monkeys: Their Ecology, Behavior and Evolution. Cambridge University Press, Cambridge: 229–249.

Kemp T.S. 2005. The Origin and Evolution of Mammals. Oxford University Press, Oxford, 331 p. https://doi.org/10.1093/oso/9780198507604.001.0001

Kinnear J.E., Cockson A., Christensen P. and Main A.R. 1979. The nutritional biology of the ruminants and ruminant-like mammals – a new approach. Comparative Biochemistry and Physiology, Ser. A, 64: 357–365. https://doi.org/10.1016/0300-9629(79)90455-9

Kotze S.H., Van der Merwe E.L., Bennett N.C. and O’Riain M.J. 2010. The comparative anatomy of the abdominal gastrointestinal tract of six species of African mole-rat (Rodentia, Bathyergidae). Journal of Morphology, 271: 50–60. https://doi.org/10.1002/jmor.10778

Kuznetsov G.V. 2006. Mammals of Vietnam. KMK Scientific Press, Moscow, 420 p. [In Russian].

Langer P. 1980. Stomach evolution in the Macropodidae Owen, 1839 (Mammalia: Marsupialia). Zeitschrift für Zoologische Systematik und Evolutionsforschung, 18: 211–232. https://doi.org/10.1111/j.1439-0469.1980.tb00740.x

Langer P. 1988. The Mammalian Herbivore Stomach. Comparative Anatomy, Function and Evolution. Gustav Fischer, Stuttgart and New York, 557 p.

Langer P. 1991. Evolution of the digestive tract in mammals. Verhandlungen der Deutschen Zoologischen Gesellschaft, 84: 169–193.

Lee W.B. and Houston D.C. 1995. The rate of change of gut anatomy in voles in relation to diet quality. Journal of Zoology, 236: 341–345. https://doi.org/10.1111/j.1469-7998.1995.tb04500.x

Ley R.E., Hamady M., Lozupone C., Turnbaugh P.J., Ramey R.R., Bircher J.S., Schlegel M.L., Tucker T.A., Schrenzel M.D., Knight R. and Gordon J.I. 2008. Evolution of mammals and their gut microbes. Science, 320: 1647–1651. https://doi.org/10.1126/science.1155725

Luckett W.P. and Hartenberger J.-L. 1993. Monophyly or polyphyly of the Order Rodentia: possible conflict between morphological and molecular interpretations. Journal of Mammalian Evolution, 1: 127–147. https://doi.org/10.1007/BF01041591

MacFadden B.J. 2000a. Origin and evolution of the grazing guild in Cenozoic New World terrestrial mammals. In: H.-D. Sues (Ed.). Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the Fossil Record. Cambridge University Press, Cambridge: 223–244. https://doi.org/10.1017/CBO9780511549717.009

MacFadden B.J. 2000b. Cenozoic mammalian herbivores from the Americas: reconstructing ancient diets and terrestrial communities. Annual Review of Ecology and Systematics, 31: 33–59. https://doi.org/10.1146/annurev.ecolsys.31.1.33

Mackie R.I. 2002. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integrative and Comparative Biology, 42: 319–326. https://doi.org/10.1093/icb/42.2.319

Marivaux L., Vianey-Liaud M., Welcomme J.-L. and Jaeger J.-J. 2002. The role of Asia in the origin and diversification of hystricognathous rodents. Zoologica Scripta, 31: 225–239. https://doi.org/10.1046/j.1463-6409.2002.00074.x

Marivaux L., Chaimanee Y., Yamee C., Srisuk P. and Jaeger J.-J. 2004. Discovery of Fallomus ladakhensis Nanda and Sahni, 1998 (Mammalia, Rodentia, Diatomyidae) in the lignites of Nong Ya Plong (Phetchaburi Province, Thailand): systematic, biochronological and paleoenvironmental implications. Geodiversitas, 26: 493–507.

Millien V. 2006. Morphological evolution is accelerated among island mammals. PloS Biology, 4: 1863–1868. https://doi.org/10.1371/journal.pbio.0040384

Millien V. 2008. The largest among the smallest: the body mass of the giant rodent Josephoartigasia monesi. Proceedings of the Royal Society, Ser. B, 275: 1953–1955. https://doi.org/10.1098/rspb.2008.0087

Musser G.G., Lunde D.P. and Son N.T. 2006. Description of a new genus and species of rodent (Murinae, Muridae, Rodentia) from the Tower Karst region of Northeastern Vietnam. American Museum Novitates, 3517: 1–41. https://doi.org/10.1206/0003-0082(2006)3517[1:DOANGA]2.0.CO;2

Naumova E.I. and Zharova G.K. 2003. Structure and functions of the digestive tract in the maned hamster Lophiomys imhausi. Zoologicheskii Zhurnal, 82: 1368–1374. [In Russian].

Nomina Anatomica Veterinaria. 2005. 5th ed. Publ. Edit. Comm. I.C.V.G.A.N., Hannover et al., 166 p.

Panteleyev P.A., Terekhina A.N. and Varshavsky A.A. 1990. Ecogeographic variation in rodents. Nauka, Moscow, 374 p. [In Russian].

Perrin M.R. and Curtis B.A. 1980. Comparative morphology of the digestive system of 19 species of Southern African myomorph rodents in relation to diet and evolution. South African Journal of Zoology, 15: 22–33. https://doi.org/10.1080/02541858.1980.11447680

Retallack G.J. 2001. Cenozoic Expansion of Grasslands and Climatic Cooling. Journal of Geology, 109: 407–426. https://doi.org/10.1086/320791

Sallam H.M., Seiffert E.R., Steiper M.E. and Simons E.L. 2009. Fossil and molecular evidence constrain scenarios for the early evolutionary and biogeographic history of hystricognathous rodents. Proceedings of the National Academy of Sciences, U.S.A., 106: 16722–16727. https://doi.org/10.1073/pnas.0908702106

Sanchez-Villagra M.R., Aguilera O. and Horovitz I. 2003. The anatomy of the World’s largest extinct rodent. Science, 301: 1708–1710. https://doi.org/10.1126/science.1089332

Schmidt-Kittler N., Vianey-Liaud M. and Marivaux L. 2007. Oligocene–Miocene Vertebrates from the Valley of Lakes (Central Mongolia): Morphology, phylogenetic and stratigraphic implications 6. The Ctenodactylidae (Rodentia, Mammalia). Annalen des Naturhistorischen Museums in Wien, 108 A: 173–215.

Seebeck J.H. and Rose R.W. 1989. Potoroidae. In: D.W. Walton and B.J. Richardson (Eds.). Fauna of Australia. Australian Government Publishing Service, Canberra, 1B: 716–739.

Shvarts S.S. 1977. The Evolutionary Ecology of Animals. Consultants Bureau, New York, 292 p.

Shvarts S.S., Smirnov V.S. and Dobrinsky L.N. 1968. Method of morphophysiological indicators in the ecology of terrestrial vertebrates. Proceedings of the Institute of the Ecology of Animals and Plants (Sverdlovsk), 58: 1–387. [In Russian].

Simpson G.G. 1944. Tempo and Mode in Evolution. Columbia University Press, New York, 237 p.

Simpson G.G. 1980. Splendid Isolation: The Curious History of South American Mammals. Yale University Press, New Haven and London, 266 p.

Stevens E. and Hume I.D. 1995. Comparative Physiology of the Vertebrate Digestive System. Cambridge University Press, Cambridge, 400 p.

Stromberg C.A.E. 2005. Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proceedings of the National Academy of Sciences, U.S.A., 102: 11980–11984. https://doi.org/10.1073/pnas.0505700102

Tullberg T. 1899. Ueber das System der Nagethiere: eine Phylogenetische Studie. Nova Acta Regiae Societatis Scientiarum Upsaliensis (Upsala), 18: 1–514. https://doi.org/10.5962/bhl.title.1733

Veloso C. and Bozinovic F. 1993. Dietary and digestive constraints on basal energy metabolism in a small herbivorous rodent. Ecology, 74: 2003–2010. https://doi.org/10.2307/1940843

Vorontsov N.N. 1963. Irregularity of tempo of organ transformation and the principle of the compensation of functions. Zoologicheskii Zhurnal, 42: 1289–1305. [In Russian].

Vorontsov N.N. 1979. Evolution of the Alimentary System in Myomorph Rodents. Smithsonian Institution Publ., Washington, D.C. and Nat. Sci. Foundation, 346 p.

Vorontsov N.N. 1982. Nizshie khomyakoobrasnye (Cricetidae) mirovoy fauny: morfologiya i ekologiya [Primitive Cricetids (Cricetidae) of the World Fauna: Morphology and Ecology]. Nauka, Leningrad, 451 p. [In Russian].

Young Owl M. 1994. A direct method for measurement of gross surface area of mammalian gastro-intestinal tract. In: D.J. Chivers and P. Langer (Eds.). The Digestive System in Mammals: Food, Form and Function. Cambridge University Press. Cambridge: 219–233. https://doi.org/10.1017/CBO9780511661716.015

Wilson D.E. 2009. Class Mammalia (Mammals). In: D.E. Wilson and R.A. Mittermeier (Eds.). Handbook of the Mammals of the World. Lynx Edicions, Barcelona, 1: 18–47.

 

© Zoological Institute of the Russian Academy of Sciences
Last modified: March 25, 2024