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

Lead Research Organisation: University of Edinburgh
Department Name: The Roslin Institute

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).

Publications

10 25 50
 
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 power of 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, contains a large component of growth potential and is not always related to behaviour. In this regard AGRP does not change in situations were animals are fed a diluted diet that controls the growth curve but can be fed ad libitum . Pancreatic genes, including APP, have so far the most reliable peripheral responses to the levels of restriction applied. This appears to differ in many regards with what we have seen in mammals. Using the samples generated in these studies it has been possible for a PhD student to develop new hypothesis on the role of PYY in the pancreas and the distribution and response of gastrin and CCK in the gut.
A particularly exciting finding has been the correlation between sex, growth potential and AGRP expression . This and a similar experiment using a different form of dietary dilution established that dietary dilution at a level allowing ad libitum feeding had no impact on AGRP levels despite producing gross changes in feeding behaviour.
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 dilution but rely 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, may well be key for setting the growth rate and may offer a route to ultimately controlling growth. If the pathways that set this level of expression can be dissected this may be important. The final experiments will go some way to starting that process. A PhD student is now developing these approaches in collaboration with a broiler breeder company.
The exciting observations on sex effects on the feeding centre have suggested further experiments that we executed . This has lead to some exciting implications of how body weight ( or its set point) is governed genetically. The paper on this is has been published and we intend to pursue this line of research in the future and the results are proving exciting.
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 feed restriction in broiler breeders. Currently the methods developed in this project are being used in a CASE studentship with a breeding company to evaluate practical strategies to address feed restriction in broiler breeders. So this demonstrates a bridge from science to practice.
First Year Of Impact 2013
Sector Agriculture, Food and Drink,Construction
Impact Types Societal

 
Description 3rd Joint Meeting between the French and British 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 data '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 Can looking into the brain help us solve the paradox of the broiler breeder chicken? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Talks and debates on the five freedoms. 2015 marks 50 years since the publication of the Brambell report, which inspired the key criteria of modern day animal welfare; namely the Five Freedoms.

This event marked the occasion. There was lively debate and questions and the audience covered a wide range of practioners and industry in the field of animal welfare.
Year(s) Of Engagement Activity 2015
URL http://www.sruc.ac.uk/events/event/355/animal_welfare_day_50_years_of_animal_welfare_science
 
Description Industry academia conference (Towards the chicken of the future, RVS) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Discussion on the direction of selection and the way that science can support the demands to produce more meat

Interaction with a range of public bodies, industry and welfare pressure groups.
Year(s) Of Engagement Activity 2014
URL http://www.rvc.ac.uk/Meetings/chicken-of-the-future/Index.cfm
 
Description OPEN day 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact To introduce our work on the sustainability of poultry and egg production to a wider audience. We had a number of activities which introduced the role of the cuticle in preventing bacterial penetration of the egg. For many people this was a revelation. It allowed an opening to discussions on modern farming and to challenge many misconceptions. There was also a lot of hands on opportunities. The event was so successful that we have developed it into a grant for building kits for using at farm visits.
Year(s) Of Engagement Activity 2016
URL http://www.bbsrc.ac.uk/news/people-skills-training/2016/160107-pr-farm-science-at-open-farm-sunday/
 
Description Presentation at British NeuroEndocrine Group (Glasgow) CCKAR 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other audiences
Results and Impact Communication with a wide range of non-avian scientists working on appetite
Year(s) Of Engagement Activity 2016
 
Description Presentation at International Symposium Avian Endocrinology (Niagara on the Lake) CCKAR 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Communication beyond poultry to wild bird and ecological researchers
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description Presentation at International Symposium Avian Endocrinology (Niagara on the Lake) MSH 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Communication beyond poultry to wild bird and ecological researchers
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description Presentation at International Symposium Avian Endocrinology (Niagara on the Lake) Sex 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Communication beyond poultry to wild bird and ecological researchers
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description STEM 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact School event for Careers advice. Many questions about nature and topic of work discussed, sparked interest in future careers in science.
Year(s) Of Engagement Activity 2015,2016
 
Description Science access for schools 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Schools
Results and Impact Science Insights students spend short periods of time hosted by a number of different researchers, giving them an insight into a wide variety of research

There was positive feedback and hopefully some students will take a biological science path
Year(s) Of Engagement Activity 2014
URL http://www.scienceinsights.ed.ac.uk
 
Description Tissue distribution and dynamic regulation of chicken peptide YY (PYY) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact 18th International Congress of Comparative Endocrinology , Communication of work by PhD student which as will be apparent from the URL was a great learning and confidence building experience
Year(s) Of Engagement Activity 2017
URL https://goabroadfund.wordpress.com/2017/10/23/18th-international-congress-of-comparative-endocrinolo...