Investigating how the type and quantity of food affect foraging behaviour and the neural circuits controlling feeding in broiler breeder chickens

Lead Research Organisation: Newcastle University
Department Name: Sch of Biology

Abstract

The 54 billion chickens produced each year for their meat (broilers) provide a third of global meat consumption. Chicken provides high quality protein, preventing human malnutrition and with the global demand for meat growing as people become richer, chicken meat plays an important role in food security. Chicken is also efficient to produce requiring lower food inputs per kg produced, reducing its carbon footprint compared to other meats.

Because of scientific breeding methods, broiler chickens now grow 3 times faster than they did 50 years ago, reaching their 2.5 kg slaughter weight as juveniles at just 6 weeks old. This success has come at a welfare cost to the parents of broilers, known as broiler breeders (estimated 350 million birds per year globally). Broiler breeders reach sexual maturity at 20 weeks and reproduce until 60 weeks of age. Because they have almost the same potential for rapid growth as broilers, they must be food restricted to control their growth, otherwise they become obese, infertile, and unhealthy and many would die. But with their food ration restricted to one-third of what they could eat, broiler breeders finish their food in minutes and then pace, forage and peck at non-food objects, and will work hard to get more food. All of which suggests they are suffering negative welfare in terms of hunger.

The fact that both generous and restricted feeding result in welfare problems creates an ethical dilemma known as 'the broiler breeder paradox'. One potential solution is to restrict growth ensuring good health but reduce hunger by providing a more 'filling' food. Adding dietary fibre makes food less energy-dense, so a larger volume of food results in the same total energy intake. This food takes longer to eat and digest, and behaviour appears more normal, but does it reduce hunger and improve welfare? This project aims to help us answer this question.

As well as watching how behaviour is changed by different diets, we will use two new approaches to measure the welfare impact of broiler breeder hunger:

1) A foraging motivation test which measures how much the bird wants to forage (peck and scratch) in a new location without providing food. Because no food is provided, this test measures hunger without affecting it.
2) Measuring the body's systems in the gut (nerve signals and hormones) and in a part of the brain which control eating behaviour (the hypothalamus), where our focus will be on a substance called agouti-related protein (AGRP). We have shown that AGRP can be used as a measure of hunger in chickens: AGRP depends on the amount of food eaten in both the long-term (over several weeks) and the short term (in the last few days). We also suspect, based on a small experiment, that restricting growth using a high fibre diet might reduce AGRP compared to the usual rationed food.

We will apply these measures in combination to ask the following questions:

1) How do our different measures of hunger vary, meal to meal and over the day?
2) How is hunger affected by adding dietary fibre to reduce energy density?
3) How are different signals about 'fullness' from the chickens' gut integrated by the brain?
In the final part (4) we will apply what we have learnt. We will test whether new broiler breeder diets developed by an international poultry breeding company can reduce hunger and improve welfare. Our project will therefore help the chicken industry to respond to the ethical concerns in society over a difficult aspect of animal welfare.

Finally, as food intake regulation is largely similar in birds and mammals, our findings will be of interest to those aiming to reduce obesity in humans. In particular, our investigation of dietary changes to reduce energy intake while promoting 'fullness' and reducing hunger, is relevant to 'dieting' for weight loss in humans.

Technical Summary

Broiler breeder chickens are food restricted to ensure good reproduction and health, but the resulting hunger is a welfare problem. Restriction of energy intake and growth by providing more of a lower energy density food (e.g. high dietary fibre) might reduce hunger. To determine this requires a better understanding of how the brain integrates information about the energy content and other aspects affecting satiety such as gut fill, and how this affects behaviour and feeding motivation.

The arcuate nucleus of the hypothalamus is key to the regulation of energy intake: AGRP mRNA is an integrated measure of hunger being responsive i) to both short and long term aspects of food intake, and ii) to manipulations of energy density. In a series of experiments, we will measure different variables relating to hunger in the same birds: i) home pen behaviour ii) foraging motivation by imposing a natural cost (of walking through water) on access to a foraging area without food (which avoids altering the hunger state). iii) expression of AGRP and related neuropeptides and receptors (POMC, CCKAR) iv) expression of gut hormone genes (CCK, Ghrelin, MCH, GLP-1).

We will investigate:
1) Diurnal and meal to meal variation using three feeding treatments (ad libitum (AL), am- and pm-fed rationed (R) birds) and sampling at 1,8 or 24hrs after feeding.
2) The effect of different levels of energy density will be identified by comparing R and AL fed controls with birds fed two different levels of dietary fibre (oat hulls) but with the same total energy intake and growth as R birds.
3) To identify how gut signals affect the arcuate nucleus, i) A model system using a standardised dietary fibre will be developed ii) the effect of crop or proventricular vagotomy will be separately compared iii) the effect of a CCKAR antagonist will be determined.
4) Commercially-relevant diets provided by a poultry breeding company will be tested to determine their effects on our hunger variables.

Planned Impact

The poultry industry provides a major part of the world's protein in an efficient manner. However there are issues surrounding the breeding birds' management where research on the issue of how to control their growth whilst reducing the symptoms of hunger is required. This project will address the 'broiler breeder paradox', where food restriction is required to ensure the animals' welfare but the resulting hunger is seen as a welfare issue.

The principal benefit from this research will be a greater understanding of how diluting diets with fibre can improve welfare by producing satiety or a feeling of fullness. The project will deliver validated behavioural and physiological measurements of hunger and greater understanding of the way in which satiety and hunger in birds are controlled. We expect that by the end of the project we will have a clear assessment of whether fibre dilution does produce a signature of satiety in the brain and if commercially relevant diets can improve welfare. This will aid the poultry industry in identifying diets which enhance satiety and would represent a step towards solving the broiler breeder paradox.

This work will benefit the birds themselves, responding to societal concerns over animal welfare issues in intensive animal production systems. It will also help address an aspect of poultry production the industry itself would like to improve. The industry will benefit directly from the final part of the project where we will use the methods and knowledge developed to test the potential satiety benefits of practical diets developed by a major poultry breeding company. Our findings will enable breeding companies to implement changes in their dietary recommendations to producers. More generally, the methods and knowledge developed will enable the welfare benefits of other diluted diets or alternative feeding strategies to be appraised. This will be of interest to other stakeholders interested in the welfare of broiler breeders, such as animal welfare charities (e.g. RSPCA), pressure groups (e.g. CIWF) and other expert groups that advise policy makers (The Farm Animal Welfare Committee, European Food Standards Agency) and policy makers themselves (e.g. Defra).

The basic understanding of how dietary fibre can affect gut fill, inducing satiety, has potential impact beyond birds and as with many discoveries in the field of nutrition the chicken can be an excellent model. So in the efforts to fight obesity in humans and companion animals these findings have wider potential applications than the immediate target of the work.

We have a strong record of communication of our work to industry and other stakeholders through various routes. As well as presenting at discipline-specific academic conferences, we will target applied scientific conferences such as those of the WPSA which typically comprise 50% industry and 50% academia. We will also publish results in industry publications such as Poultry World (Deliverable 5) and produce a policy briefing made available on the Knowledge Scotland website (Deliverable 6). To ensure wider dissemination appropriate industry days and agricultural events (Pig and Poultry Fair; Deliverable 2) will be used along with a specific meeting organised to target the full range of organisations with an interest in this topic (Deliverable 3). This will be publicised through invitations to relevant contacts but also through web material and a press release (Deliverable 1), and summaries made available afterwards (Deliverable 4).
 
Description The marker of hunger, AGRP, is affected only minimally by daily changes due to time of day or relationship to feeding time. However because of the large sample sizes in the experiments performed we are able to see effects of food intake on the 'anorectic' neurones with effects on POMC becoming evident. There is growing evidence from the body of work that POMC may be the more reliable indicator of the behavioural outcome. Unfortunately larger sample sizes are required to reliably detect the differences. The body of work is suggesting that AGRP expression in many, but not all situations, reflects a large component of growth potential and is not always related to feeding behaviour. In this regard, AGRP mRNA does not change in situations where animals are fed a diluted diet that controls the growth rate but can be fed ad libitum. Pancreatic genes including pancreatic polypeptide have so far provided the most reliable markers of the levels of food restriction applied. A particularly significant finding has been a correlation between sex, growth rate and AGRP gene expression for which there is little information available in birds and other vertebrates. A more detailed analysis of the full behavioral components of the experiments is yet to be completed.
Exploitation Route The results have been used in studies to investigate alternative feeding strategies for broiler breeder hens. These differ in that they do not rely purely on dietary dilution but also on the balance of energy and protein to control growth. The markers developed will be used in those studies. The realisation that AGRP levels, whilst not responding to methods that produce apparent satiety and reduce growth, they may offer a route to controlling growth rate. If the pathways that set this level of expression for growth can be dissected, this may be important. The final experiments by collaborators on the project will help to start this process and we have had collaborative interest from a broiler breeder company in this regard.
Sectors Agriculture, Food and Drink

URL https://www.youtube.com/watch?v=UudL-Y9-5Ts
 
Description The methods developed have allowed us to evaluate alternative feeding strategies to improve broiler breeder welfare. The experimental basis for the project has already been communicated to DEFRA. It is likely that the more recent studies will allow a logical approach to the issue of food restriction in broiler breeders. The work has attracted interest from a food additives company setting the stage for future industrial collaboration.
First Year Of Impact 2013
Impact Types Societal

 
Description 3rd Joint Meeting between the British and French Neuroendocrine Societies, Lille, September 2015. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presentation of poster 'Sex differences in basal hypothalamic anorectic and orexigenic gene expression after re-feeding. Caughey S, Wilson PW, Mukhtar N, D'Eath RB, Dunn IC, Boswell T'. Discussion with scientists in the food intake field and discussions on its meaning.
Year(s) Of Engagement Activity 2015
URL http://hypothalamus.eu/wp-content/uploads/SNE-BSN_2015_Preliminary-Program-1.pdf
 
Description The 11th International Symposium on Avian Endocrinology Poster 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Poster: Sex differences in basal hypothalamic anorectic and orexigenic gene expression after
re-feeding with normal and non-nutritive diets. Sarah Caughey, Peter Wilson, Nasir Mukhtar, Rick
D'Eath, Ian Dunn, Tim Boswell. Communication to poultry researchers and beyond to wild bird researchers.
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description The 11th International Symposium on Avian Endocrinology Talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited Symposium talk: 'Control of food intake by the central melanocortin system and its
feedback regulation'. Timothy Boswell, Sarah Caughey, Peter Wilson, Richard
D'Eath, Ian Dunn. Communication to poultry research and beyond to wild bird researchers
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description The 27th Conference of European Comparative Endocrinologists Rennes 2014 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited Symposium talk: 'Leptin and the regulation of the melanocortin system in birds'. Boswell T. Consideration of how mechanisms controlling food intake differ between vertebrates.
Year(s) Of Engagement Activity 2014
URL https://cece2014.wordpress.com/