Energy Expenditure

Limits to sustained energy expenditure

The maximum rate at which animals can expend energy is an important conceptual constraint on the level at which animals can perform – in the sense of their ability to process energy that can be used for either survival (eg thermogenesis in extreme cold) or for reproduction.

In many circumstances animals may be extrinsically limited in the supplies of energy which will place ceilings on the levels of performance. Obvious examples are animals when animals are forced to hibernate to conserve energy over periods when there is scant food availability in the environment.

In many circumstances however it seems that the supply of energy in the environment is probably not limited. In these circumstances animals probably routinely run up against limitations in their own physiology that constraint their capacity to process energy – intrinsic limits.

Because understanding these limits has important implications for our understanding of how animals function in the wild there as been intense interest in understanding what the physiological factors imposing such limits might be. We are using lactating mice a s a model system to try to unravel what imposes these physiological limitations on animals and what the implications of these limits are in an ecological context.

 In the 1980s Serge Daan and Rudi Drent at the University of Groningen suggested that maximal performance was in some way linked to the basal rate of metabolism. This is because both traits may be related to the capacity of the alimentary tract to process energy. If an animal has a large alimentary tract that is very metabolically active it can digest large quantities of food, but at the same time must pay high resting costs to maintain that digestive system. This led to the so called ‘central limitation hypothesis’ – that energy processing via the alimentary tract provides a common limit on all processes and provides a link between DEE and BMR.

 In the 1990s several studies were made on lactating mice as a model system to explore the limitations on the energy processing capacity particularly by Kim Hammond and Jared Diamond at UCLA. These studies revealed that when mice were placed under a combination of energetic loads (lactation and cold exposure for example) they were occasionally able to upregulate their intake. This suggested that the limitations in the system were actually being imposed not at the gut but in the metabolic capacity of other tissues where energy as ultimately processed. This was called the ‘peripheral limitation’ hypothesis. Kim Hammond suggested that in lactating mice these limits were actually imposed by the capacity of the mammary glands to secrete milk.

The fact mice would not eat additional food when given more pups to raise or when lactation was artificially extended but would do so when forced to lactate in the cold was thus interpreted to be because when lactation was extended or litter size increased the mice the animals were already working at the capacity of their mammary tissues to deliver milk so even if they had eaten more energy they couldn’t use it. However, when placed in the cold they could use the extra energy for thermogenesis and promptly elevated their intake accordingly.

 Following an initial paper in 1996 on lactating mice we developed a model system to explore these ideas and in 2001 published a series of papers which essentially replicated much of the work that had been previously done by Hammond and Diamond but in a different mouse strain (the MF1 mosue). The essential difference between our work and that of Kim Hammond however was that we actually measured the milk production using our expertise in isotope measurements. The results were surprising because they suggested that not only did mice in the cold upregulate their intake but they also elevated their milk production and produced by consequence larger pups.

This observation was fundamentally incompatible with the suggestion that the limits were imposed by a processing limit in the mammary gland – as the mice had clearly upregulated their milk intake. Puzzlingly they had not done this when litter size was increased but rather when they were placed under an additional external load of cold exposure.

In 2003 we published an additional series of 3 papers which examined the responses of mice to hot 9thermoneutral conditions). In this situation animals did the opposite to those in the cold. They ate less but produced les milk leading to fewer and smaller pups.

To understand these data we proposed a completely novel hypothesis for the factor imposing the limitation. This was the ‘heat constraint hypothesis’. Our suggestion is that at peak lactation mice are constrained by their internal heat production and risk of hypothermia. Thus imposing extra demands on mice at room temperature does not impel them to eat more food because they are already working at the limits that are imposed by their capacity to lose heat.

When these animals are place din the cold however we do not give them an extra load – we remove the heat constraint. The cold allows them to lose more heat and thus they can increase their milk production (which generates additional heat) and this has the knock on effects of generating larger pups and requiring more energy intake – hence they elevate their food consumption. Conversely in the hot conditions the capacity to generate heat was diminished leading to reduced milk production, smaller offspring and lower food intake.

 Our current experiments aim to test this hypothesis by manipulating heat production and capacity to lose heat without altering the ambient temperature. In particular we are shaving mice at peak lactation to relieve them of heat stress and measuring if they respond to this shaving by elevating their heat production by producing more milk and thus larger pups.

One mechanism that may impose the heat limitation is that the pups huddled around the mother, when suckling, may cause her to overheat and thus discontinue the suckling bout. In hot conditions she would heat up more rapidly and thus terminate more quickly disrupting the sucking stimulus which plays a key role in sustaining milk production. To test this idea we are using passive implanted transponders (Minimitter vital view system) which monitors the body temperature of mice continuously. By correlating the temperature of the mother with her suckling behaviour we can examine directly whether she terminates suckling bouts as she approaches a critically high body temperature.

An example track of the body temperature of a lactating mouse over the last 25 minutes of a suckling bout during the last 3 days of lactation is shown in the above figure. This track is consistent with the idea that the mouse terminated its suckling because it experienced hyperthermia. By examining many such tracks we hope to establish the role that this mechanism may play in mediating the heat constraint on lactating mice.

One hypothesis derived from the framework established by Drent and Daan is that variations in basal metabolic rate will be linked to variation in both morphology and sustained energy intake or maximal sustained metabolic rate. In turn this should lead to associations between BMR and aspects of performance that might be linked to sustained metabolic rate and intake such as reproductive capacity. We have been exploring these ideas by seeking associations between these traits at the phenotypic level.

Figure A shows the correlations between morphological aspects of a lactating mouse (at the top), RMR in the centre of the diagram and at the bottom sustained maximal metabolic rate and reproductive output. Although RMR is linked to the sizes of the liver and alimentary tract, plus the size of the mammary gland the association between RMR and sustained energy intake is very weak. In B the same figure is shown but with any effects due to body mass removed. Once this is performed almost all the associations disappear. Sustained energy intake is associated with reproductive performance but all the linkages between these two parameters and either morphology or RMR are no longer significant.

In 2010 we published a wide ranging review that explored the consequences of heat dissipation limitation for our understanding of the whole area of animal energetics. The paper was published in the Journal of Animal Ecology (online on 28th April 2010) and has been ranked on the f1000 biology site as 'exceptional'.


Pdfs for most of the following publications are available for free download here. 

  • SPEAKMAN, J.R. and McQueenie, J. (1996)
    Limits to sustained metabolic rate: The link between food intake, basal metabolic rate, and morphology in reproducing mice, Mus musculus.
    Physiological Zoology 69 Iss 4: 746-769.
  • SPEAKMAN, J.R. and Johnson, M.S. (2000)
    Relationships between resting metabolic rate and morphology in lactating mice: what tissues are the major contributors to resting metabolism? In ‘Living in the Cold: vol III’ Edited by G. Heldmaier and M. Klingenspor. Springer Berlin.
  • Johnson, M.S., Thomson, S.C. and SPEAKMAN, J.R. (2001)
    Limits to sustained energy intake I. Lactation in the laboratory mouse Mus musculus.
    Journal of Experimental Biology 204 Iss 11: 1925-1935.
  • Johnson, M.S., Thomson, S.C. and SPEAKMAN, J.R. (2001)
    Limits to sustained energy intake II. Inter-relationships between resting metabolic rate, life-history traits and morphology in Mus musculus.
    Journal of Experimental Biology 204 Iss 11: 1937-1946.
  • Johnson, M.S., Thomson, S.C. and SPEAKMAN, J.R. (2001)
    Limits to sustained energy intake III. Effects of concurrent pregnancy and lactation in Mus
    Journal of Experimental Biology 204 Iss 11: 1947-1956.
  • SPEAKMAN, J.R., Gidney, A., Bett, J., Mitchell, I.P. and Johnson, M.S. (2001)
    Limits to sustained energy intake IV. Effect of variation in food quality on lactating mice
    Mus musculus.
    Journal of Experimental Biology 204 Iss 11: 1957-1965.
  • Johnson, M.S. and SPEAKMAN, J.R. (2001)
    Limits to sustained energy intake V. Effect of cold-exposure during lactation in Mus musculus.
    Journal of Experimental Biology 204 Iss 11: 1967-1977.
  • Krol, E. and SPEAKMAN, J. R. (2003).
    Limits to sustained energy intake. VI. Energetics of lactation in laboratory mice at thermoneutrality.
    Journal of Experimental Biology 206: 4255-4266
  • Krol, E. and SPEAKMAN, J. R. (2003).
    Limits to sustained energy intake. VII. Milk energy output in laboratory mice at thermoneutrality.
    Journal of Experimental Biology 206: 4267-4281
  • Krol, E., Johnson, M. S. and SPEAKMAN, J. R. (2003).
    Limits to sustained energy intake. VIII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality.
    Journal of Experimental Biology 206: 4283-4291
  • SPEAKMAN, J.R. and Krol, E. (2005)
    Limits to sustained energy intake IX: a review of hypotheses.
    Journal of Comparative Physiology B 175: 375-394
  • Selman, C., Lumsden, S., Bunger, L., Hill, W.G. and SPEAKMAN, J.R. (2001)
    Resting metabolic rate and morphology in mice (Mus musculus) selected for high and low food intake.
    Journal of Experimental Biology 204 Iss 4: 777-784.
  • SPEAKMAN, J.R., Ergon, T.E., Scantlebury, M., Reid, K.A., Cavagne, L. and Lambin, X.(2003)
    Resting metabolic rate is correlated with daily energy expenditure in free-living voles (Microtus agrestis) but reflects extrinsic rather than intrinsic limits.
    Proceedings of the National Academy of Sciences of the United States of America100: 14057-14062
  • SPEAKMAN, J.R., Krol, E. and Johnston, M.S. (2004)
    The functional significance of individual variations in BMR.
    Physiological and Biochemical Zoology 77: 900-915
  • Johnston, S., Grune, T., Bell, L., Murray, S., Souter, D., Erwin, S., Yearsley, J., Gordon, I., Illius, A., Kyriazakis, I., SPEAKMAN, J.R. (2006)
    Having it all - historical energy intakes do not generate the anticipated trade-offs in fecundity.
    Proceedings of the Royal Society of London B: Biological Sciences
  • Johnston, S.J., Souter, D.M., Erwin, S.S., Tolkamp, B.J., Yearsley, J.M., Gordon, I.J., Illius, A., Kyriazakis, I. and SPEAKMAN, J.R. (2006: in press)
    Associations between basal metabolic rate and reproductive performance in C57BL/6J mice
    Journal of Experimental Biology