Testing the ecological relevance of the heat dissipation limit hypothesis in a small mammal

Lead Research Organisation: University of Aberdeen
Department Name: School of Medical Sciences

Abstract

Everything that animals do behaviourally and physiologically requires energy. However, while there are lots of things energy can be expended on, there is only one source of that energy / food intake. If animals could eat process and expend unlimited quantities of energy there would be no problem, but of course they can't, which leads to leading to important trade-offs between competing demands within the total available budget. The maximal rate at which energy can be ingested is called the Sustained energy intake or SusEI. I have been working on the limits to SusEI and its wider ramifications for about 10 years and we have recently made a significant breakthrough in our understanding these limits. The current proposal builds on this important advance. To set this advance in context it is necessary to provide some background to the research area. Two ideas were proposed in the early 1990s concerning how limits to SusEI might be mediated. Limits might be imposed by the capacity of the alimentary tract and associated organs (the central limits hypothesis) or imposed at sites where the energy is utilised (the peripheral limits hypothesis). Over the past two years we have been working on a radically different idea, and our findings were published last year in a series of three papers in the Journal of Experimental Biology. Our hypothesis draws on agricultural observations that the performance of dairy cows is significantly affected by their capacity to dissipate heat generated during lactation. Observations we have made in laboratory mice are consistent with the hypothesis that mice similarly constrained in their capacity to dissipate heat / the heat dissipation limit hypothesis. There is, however, a problem. Laboratory mice have been selected for unusually high offspring productivity. Although the heat dissipation limitation hypothesis explains our observations in this model system, for wild small mammals, which have smaller litters, this limitation may never be reached. Establishing the ecological relevance of our observations is therefore critical before we can explore the wider ramifications of this finding. The current proposal involves work that will establish the ecological relevance of this breakthrough in our understanding of limits on SusEI of laboratory mice, therefore potentially enabling a broad spectrum of future studies. Because of the pivotal importance of SusEI, we have been able in the past to use studies of it to provide significant insights into a range of fundamentally important ecological questions. For example, understanding how climate changes influence animal distributions (Thomas, Blondell and Speakman 2001; Science; Humphries, Thomas and Speakman, 2002 Nature) and why kleptoparasitism has such an important effect on the population biology of African wild-dogs (Gorman et al 2001: Nature). The implications of understanding what limits SusEI also stretch to many other areas, including understanding the evolution of endothermy (Bennett and Ruben, 1989; Science Hayes and Garland,1996; Physiol Zool.) and the regulation of energy balance and obesity (eg Speakman et al 2002: Proc Nut Soc).

Publications

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Hambly C (2011) Measuring energy expenditure in birds using bolus injections of 13C-labelled Na-bicarbonate. in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

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Speakman JR (2011) Limits to sustained energy intake. XIII. Recent progress and future perspectives. in The Journal of experimental biology

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Speakman JR (2016) Using doubly-labelled water to measure free-living energy expenditure: Some old things to remember and some new things to consider. in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

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Vaanholt LM (2013) Limits to sustained energy intake. XIV. Heritability of reproductive performance in mice. in The Journal of experimental biology

 
Description Bank voles were used to test the Heat Dissipation hypothesis to explain why there is a limit to energy intake during peak lactation. Heat stress caused by processing food and generating milk prevents further energy intake in mice due to a risk of hypothermia. At cold temerpatures this risk is reduced and so the mother can consume more food and produce more milk.



Voles have small litters and were an important comparison to the wealth or research conducted in mice with large litters. Vole did show heat stress during peak lactation when housed at high temperatures which led to a reduction in pregancy rates and smaller litters mass and size compered to 21 deg. This corresponded to the existing mouse data. In contrast however, mice housed at cold temperatures also had smaller litters and lower reproductive sucess rates with higher pup mortailty. Animals with small litters have a trade off between the adult coping better with lactation induced heat stress during cold temperatures while the pups struggled due to their low litter mass which let to reduced success because they experienced cold stress.



This research did correspond to the heat dissipation hypothesis however it showed that animals with small litters resond differently to cold temperatures because although the mother can dissipate the heat better and produce more milk, the pups have to expend more energy keeping warm and grow at a slower rate.
Exploitation Route This work points to the importance of heat loss as a limiting factor particularly during lactation. There are two potentially important practical applications of this work. The first is for our understanding of the impacts of climate change on wild mammal populations. The second is impacts of climate change on the dairy industry
Sectors Agriculture, Food and Drink,Energy,Environment

URL http://www.abdn.ac.uk/energetics-research
 
Description Evolution of life histories : oxidative stress and immune function - costs of reproduction? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact European Society for Evolutionary Biology (ESEB) meeting, Ottawa, Canada

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
 
Description Heat dissipation and hyperthermia risk: limiting factors in the ecology of endotherms? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact SICB, Salt lake city, Utah, USA

no actual impacts realised to date
Year(s) Of Engagement Activity 2010
 
Description Limits to sustained metabolic rate 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited Keynote speaker, JEB workshop, Murren, Switzerland.

no actual impacts realised to date
Year(s) Of Engagement Activity 2010