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

Lead Research Organisation: SRUC
Department Name: Research

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 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.

Behavioural changes in restricted birds fed with diluted (high fibre) diets suggest that these diets may have minimal effects on many of the main measures of hunger/satiety, as long as the overall energy intake is restricted- these birds remain motivated to access foraging activities, and in the home pen, levels of activity and pecking remain high. There is some suggestion however that comfort behaviours (dustbathing) which are a sign of positive welfare are increased in high fibre fed birds (although not as much as in ad libitum fed birds).

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. A particularly exciting finding has been the finding of correlation between sex, growth potential and AGRP expression. This and a similar experiment using a different form of dietary dilution established that dietary dilution to allow ad libitum feeding had no impact on AGRP levels despite producing gross changes in feeding behaviour. However more detailed analysis of the full behavioural components of the experiments is still to be completed.
Exploitation Route Breeding company Aviagen have been involved in the work, and may use our results to inform their nutritional advice to producers. We continue to collaborate with them with an ongoing BBSRC studentship, which was won based on the successes of this grant.

The results have been used in the ongoing 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 they may well be key for setting the growth rate 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.
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
Impact Types Policy & public services

 
Description KTN BBSRC CASE Studentship
Amount £75,452 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 09/2015 
End 08/2019
 
Description RSPCA contract research- to compare slow and fast growing broiler strains
Amount £73,238 (GBP)
Organisation Royal Society for the Prevention of Cruelty to Animals 
Sector Charity/Non Profit
Country United Kingdom
Start 01/2018 
End 02/2019
 
Description Welfare quality assessment of the Veranda breeder housing system
Amount £19,836 (GBP)
Organisation Vencomatic Group 
Sector Private
Country Netherlands
Start 06/2016 
End 06/2019
 
Description Co-supervision and Industrial partnership for KTN BBSRC Studentship 
Organisation Aviagen Group
Country United States 
Sector Private 
PI Contribution Behaviour and physiological expertise and methods relating to understanding hunger/satiety in chickens.
Collaborator Contribution Access to chickens used in commercial feeding trials, knowledge of poultry industry 'state of the art' feeding methods and nutrition for broiler breeder chickens.
Impact No outputs as yet. Disciplines involve animal nutrition, animal breeding, neurobiology, endocrinology, animal behaviour and animal welfare
Start Year 2013
 
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 Boswell talk at 11th International Symposium on Avian Endocrinology, Niagra, Canada 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact A talk based on the research in this grant was given- reviewing what we know about appetite regulation in birds ("Control of food intake by the central melanocortin system and its feedback regulation"). Main benefit of this conference was a that it included interaction and communication beyond poultry researchers to wild bird and ecological researchers.
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description Caughey presentation at 11th International Symposium on Avian Endocrinology, Niagra, Canada 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact A talk based on the research in this grant was given- reviewing what we know about appetite regulation in birds ("Sex differences in basal hypothalamic anorectic and orexigenic gene expression after re-feeding with normal and non-nutritive diets"). Main benefit of this conference was a that it included interaction and communication beyond poultry researchers to wild bird and ecological researchers.
Year(s) Of Engagement Activity 2016
URL http://www.isae2016.ca/
 
Description Cherrie talk "The effect of different feeding strategies on female broiler breeder satiety" at ISAE UK regional meeting, 7th Feb, Bristol, UK. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Talk at UK region ISAE meeting (International society for applied ethology) on broiler breeder behaviour when fed on different alternative diets, which are relevant to the poultry industry. There was little evidence that any of these diets really improved welfare for the birds, although feeding patterns were different. Scientific discussion was stimulated in the audience.
Year(s) Of Engagement Activity 2018
URL https://www.applied-ethology.org/United_Kingdom_and_Ireland.html
 
Description D'Eath talk "Measuring hunger/satiety of broiler breeders on modified diets" at Broiler breeder paradox workshop at Poultry Welfare Symposium, Ploufragan France 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact D'Eath, R.B. and Dixon, L. 2017 Measuring hunger/satiety of broiler breeders on modified diets. Welfare implications arising from the broiler breeder paradox, Workshop at the X. Poultry Welfare Symposium, Ploufragan, France, 21st June. 8 talks by scientists and policy makers sparked discussion around a possible EU COST action to pursue solutions to various broiler breeder chicken welfare problems.
Year(s) Of Engagement Activity 2017
URL http://www.wpsa.com/index.php/calendar-home/calendar/37-xth-european-symposium-on-poultry-welfare
 
Description D'Eath talk at SRUC animal welfare day 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact D'Eath, R.B. Hunger and Obesity, Thirst and Over-drinking: The challenges of nutritional management in captive animals. SRUC's Animal Welfare Day 8th October 2015

D'Eath gave a talk at SRUC's 1 day Knowledge Transfer event on 'Animal Welfare' to coincide with World Animal Day. A wide range of interested groups represented. The talk had some general elements, but drew heavily on the research in the current grant, and Ian Dunn also spoke about current grant work at the same event.
Year(s) Of Engagement Activity 2015
 
Description Discussion with international group of Vet School Deans 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact 3rd November 2016, A group of International veterinary deans visited SRUC Edinburgh. They were from Cavite State University, Philippines, the University of the Philippines Los Baños, and The University of Bogor, Indonesia. There were 5 deans/vice deans altogether, 1 from Cavite, 2 from Los Baños and 2 from Bogor. They had interests in Farm animals (chickens and cattle), dog population management, lab animals. We also had two international staff from WAP -venertainary engagement (Thailand) and Dog population management (Philippines) and UK WAP veterinary education officer.
Laura Dixon gave them a talk and ran a trip to the Greenword building (Roslin Institute research facility) to talk about chicken research including the work of this project.
Year(s) Of Engagement Activity 2016
 
Description Dixon talk at UK/Ireland ISAE at Cork, Ireland 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Attended ISAE UK/Ireland regional meeting. Dixon presented a 20 min talk:

Dixon, L.M., Sandilands, V., D'Eath R.B. 2015 A preliminary study of resting behaviour in feed restricted and ad lib fed broiler breeders. ISAE UK & Ireland Regional Meeting, 11 Nov, Teagasc Moorepark, Fermoy, Co. Cork.

This work and preliminary data will form the basis of a BBSRC project application.
Year(s) Of Engagement Activity 2015
 
Description Talk at Indian Council Agricultural Research 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Gave a talk about the 'hungry broiler breeders' problem and our latest research in this grant to various scientists and students.
Year(s) Of Engagement Activity 2016