Rams with poor feed efficiency are highly responsive to an exogenous adrenocorticotropin hormone (ACTH) challenge

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Abstract

An animal's response to a stressor is to increase metabolic rate, and thus energy consumption through the activation of the hypothalamic–pituitary–adrenal axis. Changes to energy use by an animal are likely to influence the efficiency with which it is utilised. In this study, we tested the hypothesis that less efficient sheep are more responsive to exogenous administration of adrenocorticotropin hormone. This was done by firstly determining the appropriate dose (0.4, 1.6 or 6.4 μg/kg LW) and peak serum cortisol response time (45 min) to exogenous administration of adrenocorticotropin hormone in a pilot study (n = 3 sheep). Following this, adrenocorticotropin hormone (2.0 μg/kg LW) stimulated cortisol levels were measured in a larger group of sheep (n = 50) of known feed efficiency (feed conversion ratio and residual feed intake values). Less efficient sheep (more positive residual feed intake values) were found to have a greater (P < 0.001) increase in cortisol concentration in comparison to more efficient animals. Those sheep which had higher levels of cortisol also had a greater proportion (P < 0.001) of fat tissue. These data clearly demonstrated that efficiency of energy use, when measured as residual feed intake, is significantly related to an animal's stress response. These findings have important implications for understanding the physiological mechanisms underpinning efficiency of energy use, and may be useful in successfully identifying animals which are superior in terms of feed efficiency.

Introduction

Stress can result from either physical or physiological stressors. When an animal is exposed to a stressor, the biological response includes alterations in the animal's behaviour, neuroendocrine system, autonomic nervous system and immune system [1]. One of the key biological responses is to increase metabolic rate and energy consumption and utilisation through altering the function of the hypothalamic–pituitary–adrenal (HPA) axis [2], [3]. Metabolic rate increases because of increased catabolic processes such as increased lipolysis [4] and protein degradation [5]. Other responses to stress include behavioural changes, such as increased activity and frustration behaviour [6].

The efficiency in which an animal utilises feed for growth can be measured as residual feed intake (RFI). Residual feed intake is the difference between an animal's actual intake and its expected intake based on its live weight and growth rate over a specified period of time [7]. Luiting et al. [6] found that in chickens divergently selected for RFI, less efficient hens spent more time food pecking and displaying escape or aggressive behaviour, suggesting that they are more susceptible to stress or have less adaptive mechanisms to cope with, and adapt to, a stressor. In beef cattle divergently selected for RFI, Richardson and Herd [8] found that less efficient animals were likely to have higher basal blood cortisol levels.

Sheep, in both extensive and intensive (feedlot) production systems, are subjected to a variety of stressors including social (e.g. social hierarchy), environmental (e.g. weather, space allocation, transportation) and physiological (e.g. disease, parasite burden) stressors. An animal's total body response to stress can be measured through decreased rates of growth, decreased efficiency of nutrient utilisation for growth and a subsequent increase in the energetic cost of the animal maintaining homeostasis. It is possible that less efficient (high RFI) animals, being more sensitive to stress, or having less effective mechanisms to cope with and/or adapt to stressors, display responses more associated with chronic stress. During longer-term stress, growth is inhibited due to the chronic activation of the HPA axis and subsequent suppression of the secretion of growth hormone [25] and increased catabolism. The combination of behavioural changes and the catabolic responses to stress that result in energy mobilisation, thereby provide a mechanism by which the stress response contributes to the lower efficiency of energy utilisation by less efficient animals [9].

The objectives of this study were to firstly, determine the appropriate dose and peak serum cortisol response time for exogenous administration of ACTH and secondly, to determine whether less efficient sheep have a greater response to administration of exogenous ACTH.

Section snippets

Materials and methods

All procedures in the two studies were conducted in accordance with the guidelines set out in the “Australian Code of Practice for the Care and Use of Animals for Scientific Purposes” [10] and were approved by the Department of Primary Industries Hamilton Animal Ethics Committee.

Study 1

The effects of dose of ACTH on serum cortisol concentrations over time were plotted with fitted trendlines (Fig. 1). The fixed and random spline terms for the model used to generate the fitted trendlines are shown in Table 1. The administration of 1.6 or 6.4 μg of ACTH/kg LW resulted in a greater increase in serum cortisol concentrations over time compared to the lowest dose, but not to each other. The response to each of the three different doses of ACTH was maximised at 45 min. The mean (±S.D.)

Discussion

The change in serum cortisol concentration induced by administration of exogenous ACTH was highly related to energetic efficiency estimated by RFI. Between 35 and 40% of the variation in RFI was attributed to changes in serum cortisol concentration following administration of ACTH. This is the first time that this relationship has been demonstrated in a group of animals that had not undergone any selection pressure for RFI, and clearly indicates that variation in RFI is underpinned by

Acknowledgements

The research was funded by the Victorian Department of Primary Industries and Meat and Livestock Australia. Assistance from Peter Heazlewood, Gavin Kearney, Ian McCauley and other staff from the Victorian Department of Primary Industries at Hamilton and Attwood is greatly appreciated. S.A. Knott was in receipt of a combined Meat and Livestock Australia and The University of Melbourne postgraduate scholarship and a Department of Primary Industries Nancy Millis scholarship.

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    Present address: School of Agricultural and Veterinary Sciences, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales 2678, Australia.

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