Advertisement

Mammalian Biology

, Volume 75, Issue 2, pp 95–105 | Cite as

Ontogenetic and lung development in Tupaia belangeri during the early postnatal period

  • Kirsten FernerEmail author
  • Ulrich Zeller
  • Barthel Schmelting
  • Eberhard Fuchs
Original Investigation

Abstract

The Belanger’s tree shrew (Tupaia belangeri) has an unusual reproductive strategy. The animals are born in altricial condition and remain in the nest for the first four weeks of life, nursed only once in 48 h. This is highly demanding for the constitution of the neonates. Despite their immaturity in the external appearance at birth, newborn tree shrews have to deal with the absence of the mother. We asked if the lung structure of the neonates match the high physiological requirements of this “absentee system”. To examine the lung development of nest young tree shrews, histological and ultrastructural investigations were performed. Newborn tree shrews are at the transition stage between the saccular and the alveolar stage of lung development. In addition to small saccules, the lung has alveoli and associated structures already at birth and thus appears more mature compared with typical altricial species. The results of the present study reveal that despite their immaturity in the external appearance newborn tree shrews are relatively mature in terms of lung development. This can be interpreted as a prerequisite for thermoregulatory abilities, necessary in neonate tree shrews to cope with the restricted nature of maternal care.

Keywords

Tree shrews Neonate Lung development 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baudinette, R.V., Runciman, S.I.C., Frappell, P.F., Gannon, B.J., 1988. Development of the marsupial cardiorespiratory system. In: Tyndale-Biscoe, C.H., Janssens, P.A. (Eds.), The Developing Marsupial. Models for Biomedical Research. Springer, Berlin, Heidelberg, pp. 132–147.CrossRefGoogle Scholar
  2. Boyden, E.A., Tompsett, D.H., 1961. The postnatal growth of the lung in the dog. Acta Anat. 47, 185–215.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Brody, J.S., Vaccaro, C., 1979. Postnatal formation of alveoli: interstitial events and physiologic consequences. Fed. Proc. 38, 215–223.PubMedPubMedCentralGoogle Scholar
  4. Bronner, G.N., 1992. Notes on the early post-natal development of a giant golden mole Chrysospalax trevelyani (Günther, 1875) born in captivity (Mammalia: Insectivora; Chrysochloridae). Koedoe 35, 57–58.Google Scholar
  5. Burda, H., 1989. Reproductive biology (behavior, breeding, and postnatal development) in subterranean mole-rats, Cryptomys hottentotus (Bathyergidae). Z. Säugetierk. 54, 360–376.Google Scholar
  6. Burri, P.H., 1974. The postnatal growth of the rat lung. III. Morphol. Anat. Rec. 180, 77–98.CrossRefGoogle Scholar
  7. Burri, P.H., Dbaly, J., Weibel, E.R., 1974. The postnatal growth of the rat lung. I. Morphometry. Anat. Rec. 178, 711–730.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Butler, P.M., 1972. The problem of insectivore classification. In: Joysey, K.A., Kemp, T.S. (Eds.), Studies in Vertebrate Evolution. Oliver and Boyd, Edinburgh, pp. 253–265.Google Scholar
  9. Castleman, W.L., Lay, J.C., 1990. Morphometric and ultrastructural study of postnatal lung growth and development in calves. Am. J. Vet. Res. 151 (5), 789–795.Google Scholar
  10. Davies, P., Reid, L., Lister, G., Pitt, B., 1988. Postnatal growth of the sheep lung: a morphometric study. Anat. Rec. 220, 281–286.PubMedCrossRefPubMedCentralGoogle Scholar
  11. Dryden, G.L., 1968. Growth and development of Suncus murinus in captivity on Guam. J. Mammol. 49, 51–62.CrossRefGoogle Scholar
  12. Foresman, K.R., 1994. Comparative embryonic development of the Soricidae. In: Merritt, F., Kirkland, G.L., Rose, R.K. (Eds.), Advances in the Biology of Shrews, vol. 18. Carnegie Museum of Natural History, Special Publications, Pittsburgh, pp. 241–257.Google Scholar
  13. Fuchs, E., 1999. Tree shrews. In: Poole, T., English, P. (Eds.), The UFAW Handbook on the Care and Management of Laboratory animals. Blackwell Science, Oxford, pp. 235–245.Google Scholar
  14. Grünwald, A., Möhres, F.P., 1974. Beobachtungen zur Jugendentwicklung und Karawanenbildung bei Weißzahnspitzmäusen (Soricidae-Crocidurinae). Z. Säugetierkd. 39, 321–337.Google Scholar
  15. Gusztak, R.W., Campbell, K.L., 2004. Growth, development and maintenance of American water shrews (Sorex palustris) in captivity. Mamm. Study 29, 65–72.CrossRefGoogle Scholar
  16. Hellwing, S., 1973. The postnatal development of the white-toothed shrew Crocidura russula monacha in captivity. Z. Säugetierkd. 38, 257–270.Google Scholar
  17. Hertenstein, B., Zimmermann, E., Rahmann, H., 1987. Zur Reproduktion und ontogenetischen Entwicklung von Spitzhörnchen (Tupaia belangeri). Z. Köln. Zoo 30, 119–133.Google Scholar
  18. Hislop, A., Howard, S., Fairweather, V.I., 1984. Morphometric studies on the structural development of the lung in Macaca fascicularis during fetal and postnatal life. J. Anat. 138, 95–112.PubMedPubMedCentralGoogle Scholar
  19. Howard, C.V., Reed, M.G., 1998. Unbiased Stereology. Three-Dimensional Measurement in Microscopy. Bios Scientific Publishers, Oxford.Google Scholar
  20. Ito, T., Kanisawa, M., 1990. Endocrine cells and brush cells at the bronchio-alveolar junctions of neonatal syrian hamster lungs. J. Morphol. 206, 217–223.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Jacobsen, N.H.G., 1982. A note of mating and neonate development of the South african hedgehog (Erinaceus frontalis). Säugetierk. Mitt. 30, 199–200.Google Scholar
  22. Kahwa, C.K.B., Balemba, O.B., Assey, R.J., 2000. The pattern of ciliation and the development of the epithelial lining of the respiratory tract in the neonatal kid: a scanning electron microscopic study. Small Rum. Res. 37, 27–34.CrossRefGoogle Scholar
  23. Kaufmann, J.H., 1965. Studies on the behavior of captive tree shrews (Tupaia glis). Folia Primatol. 3, 50–74.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Kuhn, H.-J., Schwaier, A., 1973. Implantation, early placentation, and chronology of embryogenesis in Tupaia belangeri. Z. Anat. Entwickl. -Gesch. 142, 315–340.CrossRefGoogle Scholar
  25. Kuhn, H.-J., Starck, D., 1966. Die Tupaia-Zucht des Dr. Senckenbergischen Anatomischen Institutes. Nat. Mus. 96, 263–271.Google Scholar
  26. Langham, N.P.E., 1982. The ecology of the common tree shrew, Tupaia glis in peninsular Malaysia. J. Zool. London 197, 323–344.CrossRefGoogle Scholar
  27. Le Gros Clark, W.E., 1971. The Antecedents of Man. An Introduction to the Evolution of the Primates, third ed. Quadrangle Books, Chicago.Google Scholar
  28. Lechner, A.J., Banchero, N., 1982. Advanced pulmonary development in newborn Guinea pigs (Cavia porcellus). Am. J. Anat. 163, 235–246.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Luckett, W.P., 1980. Comparative Biology and Evolutionary Relationships of Tree Shrews. Plenum Press, New York.CrossRefGoogle Scholar
  30. Martin, R.D., 1968. Reproduction and ontogeny in tree shrews (Tupaia belangeri), with reference to their general behaviour and taxonomic relationships. Z. Tierpsychol. 25, 409–532.PubMedCrossRefPubMedCentralGoogle Scholar
  31. Martin, R.D., 1990. Primate Origins and Evolution: A Phylogenetic Reconstruction. Chapman & Hall/Princeton University Press, London and New Jersey.Google Scholar
  32. Mercurio, A.R., Rhodin, J.A.G., 1984. An electron microscopic study on the type I pneumocyte in the cat: postnatal morphogenesis. J. Morphol. 182, 169–178.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Müller, F., 1972. Zur stammesgeschichtlichen Veränderung der Eutheria-Ontogenesen. Re. Suisse Zool. 79, 1–97.CrossRefGoogle Scholar
  34. Puschmann, W., 2004. Zootierhaltung — Tiere in menschlicher Obhut. Verlag Harri Deutsch, Frankfurt a. M, 4. Aufl.Google Scholar
  35. Schwaier, A., 1973. Breeding tupaias (Tupaia belangeri) in captivity. Z. Versuchstierk. 15, 255–271.Google Scholar
  36. Snyder, J., Rodgers, H.F., O’Brien, J.A., Mahli, N., Magliato, S.A., Durham, P.L., 1992. Glucocorticoid effects on rabbit fetal lung maturation in vivo: an ultrastructural morphometric study. Anat. Rec. 232, 133–140.PubMedCrossRefPubMedCentralGoogle Scholar
  37. Sprankel, H., 1961. Über Verhaltensweisen und Zucht von Tupaia glis (Diard 1820) in Gefangenschaft. Z. f. wiss. Zool. 165, 186–220.Google Scholar
  38. Sterba, O., 1977. Prenatal development of selected altricial and precocial rodents. Acta Sci. Nat. Brno. 11, 1–36.Google Scholar
  39. Szdzuy, K., 2006. Reproductive Strategies of K/T-Crossing Theria: Neonate and Postnatal Development of the Morphotype of Marsupialia and Placentalia (Mammalia). Diss. Humboldt-Universität zu, Berlin.Google Scholar
  40. Szdzuy, K., Zeller, U., Renfree, M.B., Tzschentke, B., Janke, O., 2008. Postnatal lung and metabolic development in two marsupial and four eutherian species. J. Anat. 212, 164–179.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Ten Have-Oproek, A.A.W., 1981. The development of the lung in mammals: an analysis of concepts and findings. Am. J. Anat. 162, 201–219.CrossRefGoogle Scholar
  42. Vaughan, T.A., Ryan, J.M., Czaplewski, N.J., 2000. Mammalogy, fourth ed. Harcourt College Publishers, Orlando.Google Scholar
  43. Wade, P.H., 1958. Breeding season among mammals in the lowland rain-forest of North Borneo. J. Mammal. 39, 429–433.CrossRefGoogle Scholar
  44. Weibel, E.R., 1963. Morphometry of the Human Lung. Academic Press Inc., New York.CrossRefGoogle Scholar
  45. Weibel, E.R., 1967. Postnatal growth of the lung and pulmonary gas-exchange capacity. In: De Reuck, A.V.S., Porter, R. (Eds.), Development of the Lung. A Ciba Foundation Symposium. Churchill Ltd., London, pp. 131–154.CrossRefGoogle Scholar
  46. Weibel, E.R., 1970. Functional morphology of the growing lung. Respir. (Suppl.) 27, 27–35.Google Scholar
  47. Wharton, C.H., 1950. Notes on the Phillippine Tree Shrew, Urogale everetti Thomas. J. Mammal. 31, 352–354.CrossRefGoogle Scholar
  48. Winkler, G.C., Cheville, N.F., 1984. The neonatal porcine lung: ultrastructural morphology and postnatal development of the terminal airways and alveolar region. Anat. Rec. 210, 303–313.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Yates, T.L., 1984. Insectivores, elephant shrews, tree shrews, and dermopterans. In: Anderson, S., Jones, J.K. (Eds.), Orders and Families of Recent Mammals of the World. Wiley, New York, pp. 117–144.Google Scholar
  50. Zeller, U., 1983. Zur Ontogenese und Morphologie des Craniums von Tupaia belangeri (Tupaiidae, Mammalia). Diss. Med. Georg August-Universität, Göttingen.Google Scholar
  51. Zeller, U., 1986a. Ontogeny and cranial morphology of the tympanic region of the Tupaiidae, with special reference to Ptilocercus. Folia Primatol. 47, 61–80.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Zeller, U., 1986b. The systematic relations of tree shrews: evidence from skull morphogenesis. In: Else, J.G., Lee, P.C. (Eds.), Primate Evolution. Cambridge University Press, Cambridge, pp. 273–280.Google Scholar
  53. Zeller, U., 1987. Morphogenesis of the mammalian skull with special reference to Tupaia. In: Kuhn, H.J., Zeller, U. (Eds.), Morphogenesis of the Mammalian Skull. Verlag Paul Parey, Hamburg und Berlin, pp. 17–50.Google Scholar
  54. Zeltner, T.B., Burri, P.H., 1987. The postnatal development and growth of the human lung. II. Morphol. Respir. Physiol. 67, 269–282.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2009

Authors and Affiliations

  • Kirsten Ferner
    • 1
    Email author
  • Ulrich Zeller
    • 1
  • Barthel Schmelting
    • 2
  • Eberhard Fuchs
    • 2
  1. 1.Institute of Systematic ZoologyMuseum of Natural HistoryBerlinGermany
  2. 2.Clinical Neurobiology LaboratoryGerman Primate CenterGöttingenGermany

Personalised recommendations