Energy budgets of lactating and non-reproductive Brown Long-Eared Bats (Plecotus auritus) suggest females use compensation in lactation

Functional Ecology

Volumn 13, Issue 3, 1999, Pages 360-372

  McLean, J A ^a   Speakman, J R ^b  

^a SCOTTISH AGRICULTURAL COLLEGE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Doubly labelled water; Food intake; Milk; Reproduction; Tritium

Indexed keywords

PLECOTUS AURITUS;

EID: 0032801878     PISSN: 02698463     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2435.1999.00321.x     Document Type: Article

References (82)

1. Anderson, D.E. & Fedak, M.A. (1987) The energetics of sexual success of grey seals and comparison with the costs of reproduction in other pinnipeds. Symposia of the Zoological Society of London 57, 319-341.
2. Anderson, M.E. & Racey, P.A. (1991) Feeding behaviour of captive brown long-eared bats, Plecotus anritus. Animal Behaviour 42, 489-493.
3. Anthony, E.L.P. & Kunz, T.H. (1977) Feeding strategies of the little brown bat, Myotis lucifugus, in Southern New Hampshire. Ecology 58, 775-786.
4. Audet, D. & Fenton, M.B. (1988) Heterothermy and the use of torpor by the bat Eptesicus fuscus (Chiroptera: Vespertilionidae): a field study. Physiological Zoology 61, 197-204.
5. Barclay, R.M.R. (1989) The effect of reproductive condition on the foraging behaviour of female hoary bats, Lasiurus cinereus. Behavioural Ecology and Sociobiology 24, 31-37.
6. Barclay, R.M.R., Dolan, M. & Dyck, A. (1991) The digestive efficiency of bats. Canadian Journal of Zoology 69, 1853-1856.
7. Bassett, J.E. & Studier, E.H. (1988) Methods for determining water balance in bats. Ecological and Behavioural Methods for the Study of Bats (ed. T. H. Kunz), pp. 373-386. Smithsonian Institution Press, London.
8. Baverstock, P. & Green, B. (1975) Water recycling in lactation. Science 187, 657-658.
9. Bell, G.P., Bartholomew, G.A. & Nagy, K.A. (1986) The roles of energetics, water economy, foraging behaviour and geothermal refugia in the distribution of the bat, Macrotus californicus. Journal of Comparative Physiology B 156, 441-450.
10. Blaxter, K. (1989) Energy Metabolism in Animals and Man. Cambridge University Press, Cambridge.
11. Brisbin, I.L. (1966) Energy utilisation in a captive hoary bat. Journal of Mammalogy 47, 719-720.
12. Campbell, N.A. (1990) Biology, 2nd edn. Benjamin/Cummings, CA
13. Clark, B.S., Leslie, D.M. Jr & Carter, T.S. (1993). Foraging activity of adult female ozark big-eared bats (Plecotus townsendii ingens) in summer. Journal of Mammalogy 74, 422-427.
14. Clutton-Brock, T.H. (1991) The Evolution of Parental Care. Monographs in Behaviour and Ecology (eds J. R. Krebs & T. Clutton-Brock). Princeton University Press, Oxford.
15. Coutts, R.A., Fenton M.B. & Glen, E. (1973) Food intake by captive Myotis lucifugus and Eptesicus fuscus (Chiroptera: vespertilionidae). Journal of Mammalogy 54, 985-990.
16. 2O: comparisons between calorimeter and isotope values. European Nutrition Report 5, Human Metabolism, Physical Activity and Energy Expenditure, Measurements in Epidemiological Research Based on Direct and Indirect Calorimetry (ed. A. J. H. van Es), pp. 126-128. CIP-gegevens Koninklijke Bibliotheek, den Haag.
17. Darrow, J.M., Duncan, M.J., Bartke, A., Bona-Gallo, A. & Goldman, B.D. (1989) Influence of photoperiod and gonadal steroids on hibernation in the European hamster. Journal of Comparative Physiology A 163, 339-348.
18. De Fanis, E. & Jones, G. (1995) Postnatal growth, mother-infant interactions and development of vocalisations in the vespertilionid bat Plecotus auritus. Journal of Zoology 235, 291-318.
19. Ellis, W.A.H., Marples, T.G. & Phillips, W.R. (1991) The effects of a temperature-determined food supply on the annual activity cycle of the lesser long-eared bat, Nyctophilus geoffroyi Leach, 1821 (Microchiroptera: vespertilionidae). Australian Journal of Zoology 39, 263-271.
20. Entwistle, A.C., Racey, P.A. & Speakman, J.R. (1996) Habitat exploitation by a gleaning bat, Plecotus auritus. Philosophical Transactions of the Royal Society of London B Biological Sciences 351, 921-931.
21. Ewing, W.G., Studier, E.H. & O'Farrell, M.J. (1970) Autumn fat deposition and gross body composition in three species of Myotis. Comparative Biochemistry and Physiology 36, 119-129.
22. Geiser, F. & Baudinette, R.V. (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. Journal of Comparative Physiology B 157, 335-344.
23. Grinevitch, L., Holroyd, S.L. & Barclay, R.M.R. (1995) Sex differences in the use of daily torpor and foraging time by big brown bats (Eptesicus fuscus) during the reproductive season. Journal of Zoology 235, 301-309.
24. Hamilton, I.M. & Barclay, R.M.R. (1994) Patterns of daily torpor and day-roost selection by male and female big brown bats (Eptesicus fuscus). Canadian Journal of Zoology 72, 744-749.
25. Hammond, K.A. & Diamond, J. (1992) An experimental test for a ceiling on sustained metabolic rate in lactating mice. Physiological Zoology 65, 952-977.
26. Hanwell, A. & Peaker, M. (1977) Physiological effects of lactation on the mother. Symposia of the Zoological Society of London 41, 297-312.
27. Hickey, M.B.C. (1992) Effect of radiotransmitters on the attack success of hoary bats (Lasiurus cinereus). Journal of Mammalogy 73, 344-346.
28. Hickey, M.B.C. & Fenton, M.B. (1990) Foraging by red bats (Lasiurus borealis): do intra-specific chases mean territoriality? Canadian Journal of Zoology 68, 2477-2482.
29. Jenness, R. (1974) The composition of milk. Lactation - a Comprehensive Treatise. Volume III, Nutrition and Biochemistry of Milk/Maintenance (eds B. L. Larson & V. R. Smith), pp. 3-107. Academic Press, London.
30. Jenness, R. & Studier, E.H. (1976) Lactation and milk. Biology of Bats of the New World Family Phyllostomatidae, Part I (eds R. J. Baker, J. K. Jones Jr & D. C. Carter), pp. 201-218. Spec. Publishers, Mus. Texas, Technical University of Lubbock.
31. Keeler, J.O. & Studier, E.H. (1992) Nutrition in pregnant big brown bats (Eptesicus fuscus) feeding on June beetles. Journal of Mammalogy 73, 426-430.
32. Kenagy, G.J. & Barnes, B.M. (1988) Seasonal reproductive patterns in four coexisting rodent species from the Cascade mountains, Washington. Journal of Mammalogy 69, 274-292.
33. Kimball, J.W. (1983) Biology, 5th edn. Addison-Wesley, London.
34. Konig, B., Reister, J. & Markyl, H. (1988) Maternal care in house mice (Mus musculus): II. The energy cost of lactation as a function of litter size. Journal of Zoology, London 216, 195-210.
35. Kunz, T.H. (1974) Feeding ecology of a temperate insectivorous bat (Myotis velifer). Ecology 55, 693-711.
36. Kunz, T.H. (1988) Methods of assessing the availability of prey to insectivorous bats. Ecological and Behavioural Methods for the Study of Bats (ed. T. H. Kunz), pp. 191-210. Smithsonian Institution Press, London.
37. Kunz, T.H. & Nagy, K.A. (1988) Methods of energy budget analysis. Ecological and Behavioural Methods for the Study of Bats (ed. T. H. Kunz), pp. 277-302. Smithsonian Institution Press, London.
38. Kunz, T.H., Stack, M.H. & Jenness, R. (1983) A comparison of milk composition in Myotis lucifugus and Eptesicus fuscus (chiroptera: vespertilionidae). Biology of Reproduction 28, 229-234.
39. Kunz, TH., Oftedal, O.T., Robson, S.K., Kretzmann, M.B. & Kirk, C. (1995a) Changes in milk composition during lactation in three species of insectivorous bats. Journal of Comparative Physiology B. Biochemical, Systematic, and Environmental Physiology 164, 543-551.
40. Kunz, T.H., Whitaker, J.O. Jr & Wadanoli, M.D. (1995b) Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation. Oecologia 101, 407-415.
41. Kurta, A. & Kunz, T.H. (1987) Size of bats at birth and maternal investment during pregnancy. Symposia of the Zoological Society of London 57, 79-107.
42. Kurta, A., Johnson, K.A. & Kunz, T.H. (1987) Oxygen consumption and body temperature of female little brown bats (Myotis lucifugus) under simulated roost conditions. Physiological Zoology 60, 386-397.
43. Kurta, A., Bell, G.P., Nagy, K.A. & Kunz, T.H. (1989a) Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Physiological Zoology 62, 804-818.
44. Kurta, A., Bell, G.P., Nagy, K.A. & Kunz, T.H. (1989b) Water balance of free-ranging little brown bats (Myotis lucifugus) during pregnancy and lactation. Canadian Journal of Zoology 67, 2468-2472.
45. Kurta, A., Kunz, T.H. & Nagy, K.A. (1990) Energetics and water flux of free-ranging big brown bats (Eptesicus fuscus) during pregnancy and lactation. Journal of Mammalogy 71, 59-65.
46. Lifson, N.A. & McClintock, R.M. (1966) Theory of use of the turnover rates of body water for measuring energy and material balance. Journal of Theoretical Biology 12, 46-74.
47. 18O pool size determinations on the calculation of total energy expenditure. Obesity Research 3, 21-29.
48. Mattingly, D.K. & McClure, P.A. (1982) Energetics of reproduction in large-littered cotton rats (Sigmodon hispidus). Ecology 63, 183-195.
49. Mattingly, D.K. & McClure, P.A. (1985) Energy allocation during lactation in cotton rats (Sigmodon hispidus) on a restricted diet. Ecology 66, 928-937.
50. McClure, P.A. (1987) The energetics of reproduction and life histories of cricetine rodents. Symposia of the Zoological Society, London 57, 241-258.
51. McLean, J.A. & Speakman, J.R. (1997) Non-nutritional maternal support in the brown long-eared bat (Plecotus auritus). Animal Behaviour 54, 1193-1204.
52. Millar, J.S. (1987) Energy reserves in breeding small rodents. Symposium of the Zoology Society of London 57, 231-240.
53. 2 production in animals: analysis of potential errors in the doubly-labeled water method. American Journal of Physiology 238, R466-R473.
54. Nagy, K.A. & Costa, D.P. (1980) Water-flux in animals: analysis of potential errors in the tritiated water method. American Journal of Physiology 238, R454-R465.
55. Neuhauser, H.N. & Brisbin, I.L. (1969) Energy utilisation in a captive silver-haired bat. Bat Research News 10, 30-31.
56. O'Farrell, M.J., Studier, E.H. & Ewing, W.G. (1971) Energy utilisation and water requirements of captive Myotis thysanodes and Myotis lucifugus (Chiroptera). Comparative Biochemistry and Physiology 39A, 549-552.
57. Oftedal, O.T., Boness, D.J. & Tedman, R.A. (1987) The behaviour, physiology and anatomy of lactation in the Pinnipedia. Current Mammalogy 1, 175-245.
58. Perez-Jorda, J.L. (1995) Ecologia del murcielago hortelano (Eptesicus serotinus) en Andalucia. PhD Thesis, University of Seville, Seville, Spain.
59. Perrigo, G. (1987) Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Animal Behaviour 35, 1298-1316.
60. Poppitt, S.D., Speakman, J.R. & Racey, P.A. (1993) The energetics of reproduction in the common shrew (Sorex araneus): a comparison of indirect calorimetry and the doubly labelled water technique. Physiological Zoology 66, 964-982.
61. Racey, P.A. (1970) The breeding care and management of vespertilionid bats in the laboratory. Laboratory Animals 4, 171-183.
62. Racey, P.A. (1988) Reproductive assessment in bats. Ecological and Behavioural Methods for the Study of Bats (ed. T. H. Kunz), pp. 31-45. Smithsonian Institution Press, London.
63. Racey, P.A. & Speakman, J.R. (1987) The energy costs of pregnancy and lactation in heterothermic bats. Symposia of the Zoological Society of London 57, 107-125.
64. Racey, P.A., Speakman, J.R. & Swift, S.M. (1987) Reproductive adaptations of heterothermic bats at the Northern borders of their distribution. South African Journal of Science 83, 635-638.
65. Randolph, P.A., Randolph, J.C., Mattingly, K. & Foster, M.M. (1977) Energy costs of reproduction in the cotton rat. Sigmodon hispidus. Ecology 58, 31-45.
66. Ransome, R.D. (1973) Factors affecting the timing of births in the greater horseshoe bat (Rhinilophus ferrumequinum). Periodical Biology 75, 169-175.
67. Rydell, J. (1993) Variation in foraging activity of an aerial insectivorous bat during reproduction. Journal of Mammalogy 74, 503-509.
68. Slonaker, J.R. (1924) The effect of copulation, pregnancy, pseudopregnancy and lactation on the voluntary activity and food consumption of the albino rat. American Journal of Physiology 71, 362.
69. 2 production in doubly labelled water studies of animals? Functional Ecology 7, 746-750.
70. Speakman, J.R. (1997) Doubly Labelled Water: Theory and Practice. Chapman & Hall, London.
71. Speakman, J.R. & McQueenie, J. (1996) Limits to sustainable metabolic rate: the link between food intake, BMR, and morphology in reproducing mice (Mus musculus). Physiological Zoology 69, 746-769.
72. Speakman, J.R. & Racey, P.A. (1987a) The energetics of pregnancy and lactation in the brown long-eared bat, Plecotus auritus. Recent Advances in the Study of Bats (eds M. B. Fenton, P. A. Racey & J. M. V. Rayner), pp. 367-393. Cambridge University Press, Cambridge.
73. Speakman, J.R. & Racey, PA. (1987b) The equilibrium concentration of oxygen-18 in body water: implications for the accuracy of the doubly labeled water technique and a potential new method of measuring RQ in free-living animals. Journal of Theoretical Biology 127, 79-95.
74. Speakman, J.R., Catto, C.M., Webb, P.I., Swift, S.M. & Burnett, A.M. (1991) Minimum summer populations and densities of bats in north-east Scotland near the northern borders of their distributions. Journal of Zoology 225, 327-345.
75. Swift, S.M. (1980) Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in north-east Scotland. Journal of Zoology, London 190, 285-295.
76. Swift, S.M. (1981) Foraging, colonial and maternal behaviour of bats in Scotland. PhD Thesis, University of Aberdeen, Scotland.
77. Swift, S.M. (1991) Brown long-eared bat, Plecotus auritus. The Handbook of British Mammals, 3rd edn (eds G. B. Corbet & S. Harris). Blackwell Scientific Publications, Oxford.
78. Thompson, S.D. (1993) Gestation and lactation in small mammals: basal metabolic rate and the limits to energy use. Mammalian Energetics Interdisciplinary Views of Metabolism and Reproduction, (eds T. E. Tomasi & T. H. Horton), pp. 213-260. Comstock, Ithaca, NY.
79. Webb, P.I. (1992) Aspects of the ecophysiology of some vespertilionid bats at the Northern borders of their distribution. PhD Thesis, University of Aberdeen, Scotland.
80. Wilde, C.J., Kerr, M.A., Knight, C.H. & Racey, P.A. (1995) Lactation in vespertilionid bats. Symposia of the Zoological Society of London 67, 139-149.
81. Wong, W.W. & Klein, P.D. (1986) A review of techniques for the preparation of biological samples for mass-spectrometric measurements of hydrogen-2/hydrogen-1 and oxygen-18/oxy gen-16 isotope ratios. Mass Spectrometry Review 5, 313-342.
82. Wong, W.W., Lee, L.S. & Klein, P.D. (1987) Oxygen isotope ratio measurements on carbon dioxide generated by reaction of microlitre quantities of biological fluids with guanidine hydrochloride. Analytical Chemistry 59, 690-693.