Morphology and morphometry of the lungs of two East African mole rats,Tachyoryctes splendens andHeterocephalus glaber (Mammalia, Rodentia)
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Summary
The lungs of two fossorial rodents, the mole ratTachyoryctes splendens and the naked mole ratHeterocephalus glaber were investigated by transmission and scanning electron microscopy and a comparative morphometric analysis of the lungs carried out in an attempt to find out whether there are any possible structural adaptational features which may be associated with fossoriality. The data from these two ecologically disparate fossorial rodents were compared with those of surface dwelling rodents on which equivalent data are available. Morphologically, the lung ofT. splendens is essentially similar to that of terrestrial mammals while that ofH. glaber shows features of underdevelopment. InH. glaber, a cuboidal epithelium extends down the respiratory tree to line what appear to be alveolar spaces, the blood capillaries constitute a double capillary system and the type I pneumocytes have microvilli on their free surface. Morphometrically,H. glaber has notably lower values indicative of rather unspecialized lungs. While the volume density of the parenchyma is 88% inT. splendens, that inH. glaber is only 76%. The blood-gas (tissue) barrier inH. glaber is notably thicker than inT. splendens. When normalized with body weight, the surface area of the blood-gas (tissue) barrier, the pulmonary capillary blood volume, the diffusing capacities of the tissue barrier and of the whole lung are consistently appreciably lower inH. glaber. When compared withMus musculus, Rattus rattus andCavia porcellus, T. splendens has somewhat comparable values with the surface dwelling rodents but the values ofH. glaber are the lowest in the group. It is suggested thatT. splendens has not undergone full adaptation to fossoriality as is supported by its behavioural activities, particularly those of occasionally surfacing to feed and making overland excursions. The low values ofH. glaber may be commensurate with its extreme physiological adaptations for fossoriality, features which culminate in low basal metabolism and may in part explain paedomorphic traits of its respiratory system.
Keywords
Alveolar Space Terrestrial Mammal Adaptational Feature Capillary System Respiratory TreePreview
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References
- Alexander RD (1991) Some unanswered questions about naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, NJ, pp 446–465Google Scholar
- Ar A, Arieli R, Shkolnik A (1977) Blood gas properties and function in the fossorial mole rat under normal and hypoxic-hypercapnic atmospheric conditions. Respir Physiol 30:201–218Google Scholar
- Arieli R (1979) The atmospheric environment of the fossorial mole rat (Spalax ehrenbergi): effect of season, soil texture, rain, temperature, and activity. Comp Biochem Physiol 63A:569–575Google Scholar
- Arieli R, Ar A (1979) Ventilation of a fossorial mammalSpalax ehrenbergi in hypoxic and hypercapnic conditions. J Appl Physiol 47:1011–1017Google Scholar
- Arieli R, Ar A, Shkolnik A (1977) Metabolic responses of a fossorial rodent (Spalax ehrenbergi) to simulated burrow conditions. Physiol Zool 50:61–75Google Scholar
- Ayala FJ, Valentine JW (1979) Evolving: The theory and the processes of organic evolution. Benjamin Cummings, Menlo Park, CAGoogle Scholar
- Baudinette RV (1972) Energy metabolism and evaporative water loss in the California ground squirrel: effects of burrow temperature and water vapour pressure. J Comp Physiol 81:57–72Google Scholar
- Bhattia B, George S, Rao TL (1969) Hypoxia and poilikothermia in rats. J Appl Physiol 27:583–586Google Scholar
- Boggs DF, Kilgore DL, Birchard GF (1984) Respiratory physiology of burrowing mammals and birds. Comp Biochem Physiol 77A:1–7Google Scholar
- Breeze RG, Wheeldon EB (1975) The cells of the pulmonary airways. Ann Rev Respir Dis 116:705–777Google Scholar
- Brett RA (1991) The population structure of naked mole rat colonies. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the naked mole rat. Princeton (New Jersey), Princeton University Press, 97–136Google Scholar
- Burri PH (1974) The postnatal growth of the rat lung. III. Morphology. Anat Rec 180:77–98Google Scholar
- Burri PH, Weibel ER (1971) Morphometric estimation of pulmonary diffusion capacity. II. Effect pO2 on the growing lung to hypoxia and hyperoxia. Respir Physiol 11:247–264Google Scholar
- Burri PH, Weibel ER (1977) The ultrastructure and morphometry of the developing lung. In: Hodson WA (ed) Lung biology in health and disease: development of the lung. Mercel Dekker, New York, pp 215–268Google Scholar
- Chapman RC, Bennet AF (1975) Physiological correlates of burrowing in rodents. Comp Biochem Physiol 51A:599–603Google Scholar
- Chew R, Lindberg G, Hyden P (1965) Circadian rhythm of metabolic rate in pocket mice. J Mammal 46:477–494Google Scholar
- Darden TR (1970) Respiratory adaptations of a fossorial mammal, the pocket gopher (Thomomys bottae). PhD dissertation, University of California (Davis)Google Scholar
- Eloff G (1951) Adaptation in rodent moles and insectivorous moles and the theory of convergence. Nature (London) 168:1001–1002Google Scholar
- Faleschini RJ, Whitten BK (1975) Comparative hypoxic tolerance in Sciuridae. Comp Biochem Physiol 52A:217–221Google Scholar
- Forrest JB, Weibel ER (1975) Morphometric estimation of pulmonary diffusion capacity. IV. The normal guinea pig lung. Respir Physiol 24:191–202Google Scholar
- Geelhaar A, Weibel ER (1971) Morphometric estimation of pulmonary diffusion capacity. III. The effect of increased oxygen consumption in Japanese waltzing mice. Respir Physiol 11:354–366Google Scholar
- Gehr P, Mwangi DK, Amman A, Maloiy GMO, Taylor CR, Weibel ER (1981) Design of the mammalian respiratory system. IV. Scaling morphometric pulmonary diffusing capacity to body mass: wild and domestic mammals. Respir Physiol 44:61–86Google Scholar
- Gettinger RD (1975) Metabolism and thermoregulation of a fossorial rodent, the northern pocket gopher (Thomomys talpoides). Physiol Zool 48:311–322Google Scholar
- Hall FG (1965) Haemoglobin and oxygen affinities in seven species of Sciuridae. Science 148:1350–1351Google Scholar
- Hayden JS (1966) Abnormal concentrations of respiratory gases in rabbit burrows. J Mammal 47:723Google Scholar
- Hill OCW, Porter A, Bloom RT, Seago J, Southwick MD (1957) Field and laboratory studies on the naked mole ratHeterocephalus glaber. Proc Zool Soc (London) 128:455–514Google Scholar
- Hyden P, Lindberg R (1970) Hypoxia induced torpor in pocket mice (genus Perognathus). Comp Biochem Physiol 33A:167–179Google Scholar
- Jarvis JUM (1973) Activity patterns in the mole-ratsTachyoryctes splendens andHeliophobius argenteocinereus. Zool Afr 8:101–119Google Scholar
- Jarvis JUM (1978) Energetics of survival inHeterocephalus glaber (Ruppell), the naked mole rat (Rodentia: Bathyergidae). In: Schlitter DA (ed) Bulletin of Carnegie Museum of Natural History (No. 6). Pittsburgh, Trustees of Carnegie Institute, pp 81–87Google Scholar
- Jarvis JUM (1984) African mole rats. In: MacDonald D (ed) Encyclopedia of mammals, vol 2. London, Allen Unwin, pp 708–711Google Scholar
- Jarvis JUM, Sale JB (1971) Burrowing and burrow patterns of East African mole ratsTachyoryctes, Heliophobius andHeterocephalus. J Zool (London) 163:451–475Google Scholar
- Kilgore DL, Birchard GF (1980) Respiratory functions of blood in burrowing and nonburrowing birds. Am Zool 20:766–778Google Scholar
- Lovegrove BG, Wissel C (1988) Sociality in mole rats: Metabolic scaling and the role of risk sensitivity. Oecologia (Berlin) 74:600–606Google Scholar
- Maclean GS (1981) Factors influencing the composition of respiratory gases in mammal burrows. Comp Biochem Physiol 69A:373–380Google Scholar
- Maina JN (1987) The morphology of the lung of the African lungfish (Protopterus aethiopicus): A scanning electron microscopic study. Cell Tissue Res 250:191–196Google Scholar
- Maina JN, Maloiy GMO (1988) A scanning and transmission electron microscopic study of the lung of a caecilianBoulengerula taitanus. J Zool (London) 215:739–751Google Scholar
- Maina JN, King AS, Settle G (1989) An allometric study of pulmonary parameters in birds, with mammalian comparisons. Phil Trans R Soc London B 326:1–57Google Scholar
- Mayer WW (1955) The protective value of the burrow system to the hibernating Arctic ground squirrel (Spermophilus tridecemlineatus). Anat Rec 122:437–438Google Scholar
- McNab B (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47:712–733Google Scholar
- McNab B (1979) The influence of body size on the energetics and distribution of fossorial and burrowing mammals. Ecology 60:1010–1021Google Scholar
- McNab B (1988) Complications inherent in scaling the basal metabolism in mammals. Quart Rev Biol 63:25–54Google Scholar
- Meban C (1980) Thickness of the air-blood barrier in vertebrate lungs. J Anat 131:299–307Google Scholar
- Perry SF (1983) Reptilian lungs: Functional anatomy and evolution. Adv Anat Embryol Cell Biol 79:1–81Google Scholar
- Scherle WF (1970) A simple method for volumetry in organs in quantitative stereology. Mikroskopie 26:57–60Google Scholar
- Schmidt-Nielsen B, Schmidt-Nielsen K (1950) Evaporative water loss in desert rodents in their natural habitat. Ecology 31:75–85Google Scholar
- Sherman PW, Jarvis JUM, Alexander RD (1991) The biology of the naked mole-rat. Princeton (New Jersey), Princeton University PressGoogle Scholar
- Studier EH, Proctor JW (1971) Respiratory gases in burrows ofSpermophilus tridecemlineatus. J Mammal 52:631–633Google Scholar
- Thigpen LW (1940) Histology of a normally hairless rodent. J Mammal 21:449–456Google Scholar
- Tucker CE, James WE, Berry MA, Johnstone CJ, Glover RF (1976) Depressed myocardial function in the goat at high altitude. J Appl Physiol 41:356–361Google Scholar
- Weibel ER (1970/71) Morphometric estimation of pulmonary diffusion capacity. I. Model and method. Respir Physiol 11:54–75Google Scholar
- Weibel ER (1979) Stereological Methods: Practical methods for biological morphometry. London, Academic PressGoogle Scholar
- Weibel ER (1984) The pathway for oxygen. Harvard University Press, Cambridge, MAGoogle Scholar
- Weibel ER, Claassen H, Gehr P, Sehovic S, Burri P (1980) The respiratory system of the smallest mammal. In: Schmidt-Nielsen K, Bolis L, Taylor CR (eds) Comparative physiology of primitive mammals. Cambridge University Press, CambridgeGoogle Scholar
- Xu L, Mortola JP (1989) Effects of hypoxia on the lung of the chick embryo. Can J Physiol Pharmacol 67:515–519Google Scholar
- Yanav S, Buffenstein R, Jarvis JUM, Mitchell D (1989) Thermoregulation and evaporative water loss in the naked mole-rat,Heterocephalus glaber. S Afr J Sci 85:340Google Scholar