An investigation of socially-mediated emotional transfer in the chicken

Lead Research Organisation: University of Bristol
Department Name: Clinical Veterinary Science

Abstract

To ensure good animal welfare we need to identify, and then take steps to alleviate, causes of possible distress. Much research has focussed directly on physical, environmental and social situations that are distressing to laboratory or farm animals. Our proposed research takes a different angle and addresses the possibiity that animals might additionally experience distress when their own situation is good, but when they witness distress in others. In its most advanced form, this capacity might be called empathy, implying that the witness understands the reasons for its companion's distress. In humans, and perhaps great apes, such advanced abilities to understand the plight of another may promote positive social behaviour or "helping". However, the roots of empathy probably lie in a set of much simpler, building block, processes. One of these building blocks is emotional matching, also called emotional transfer or emotional contagion. These terms refer to situations where physiological or behavioural signs of distress in one animal to trigger a shared or matching response in an observer. In human infants emotional transfer is shown when the crying of one baby produces a similar crying response in others nearby.

Our recent work has shown that, under some circumstances, chickens show this type of emotional transfer. We found that mother hens react strongly and consistently (with changes in heart-rate, comb-temperature, vocalisations and other behavioural changes) when their chicks receive a mild air-puff. The aim of this research is to discover much more about the situations under which this emotional transfer takes place in chickens. The research will be useful in clarifying a field of research where results can often be over-interpreted and advanced abilities claimed when they may not really exist. But the research also has important animal welfare implications. If animals are upset by seeing distress in others this may guide our veterinary, transport or even slaughter practices. It is also possible that animals in a poor state of welfare are more likely to show emotional transfer, leading to harmful outbreaks of group panic.

We will address a number of fundamental questions in small-scale experiments with chickens:
- does the observing hen find it unpleasant to witness distress in her chicks?
- does emotional transfer occur when the observing hen is in a good emotional state herself, and when she "knows" she is in no personal danger?
- does emotional transfer help the observing hen to acquire important information about pleasant and unpleasant situations?
- to what extent does emotional transfer depend on the strength of the social relationship between the observing hen and the individual (chick or adult chicken) that receives the mildly unpleasant stimulus?
- is emotional transfer more likely if a hen is in a poor welfare state?

Taken together these studies will shed new light on the extent to which non-primate animals may share emotions. Although our laboratory studies will not directly inform policy decision on animal handling, transport or slaughter, the results will be highly relevant to these areas, and will therefore provide a platform for more applied studies on farms, laboratories and abattoirs.

Technical Summary

A conspecific observer that witnesses signs of pain or distress in another may experience an empathic emotional reaction. The word empathy refers to the vicarious transfer of emotion, but is often bound together with high level concepts such as theory of mind, and altruism. Often different levels of explanation are not differentiated in observational or experimental studies.

We have established a model whereby hens reliably show emotional transfer, responding to the mild distress of their chicks with a suite of subtle behavioural and physiological changes, detected using sensitive non-invasive recording methods. We now propose to establish the contexts, welfare consequences, and functional benefits of this emotional transfer. By so doing we will identify empathic processes that may be general to many vertebrate species, and which are likely to underpin the more complex abilities of primates and humans.

We will use place preference and other established techniques to establish whether emotional transfer is accompanied by aversion, rather than simply reflecting arousal. We will examine whether either prior emotional state, or the degree of perceived personal safety, influences the extent to which emotional transfer occurs, and whether there are any functional benefits of emotional transfer to the observer (we predict it may facilitate social aversion learning) or the demonstrator(s) (via social buffering). We will also examine how the nature and strength of the social bond between observer and demonstrator influence the degree of emotional transfer that takes place. Finally we will investigate whether the long-term welfare state of the observer influences emotional transfer.

In addition to adding to fundamental knowledge, the proposed research has direct relevance for animal welfare as little is known about whether or how distress is transmitted between farm or laboratory animals.

Planned Impact

The following are potential non-academic beneficiaries of our research.

1. Chickens. By establishing the contexts in which chickens may share mostly negative emotions we will be able to use this work as a platform for more applied investigations of the real-world impact. For example, although it takes only a few seconds to catch one chicken, it takes many hours to clear a house containing between 5000 to 50000 birds. Chickens are also loaded, shackled and stunned in sight of each other. It is even possible that the damage and injuries that chickens commonly sustain in farming systems (keel fractures affect an average of 60% of hens; up to 25% of broiler chickens can experience lameness) have some impact on their companions. None of these possibilities can be investigated without fundamental information.
2. The laying hen industry. Emotional transfer may underlie some of the common problems experienced in non-cage laying hen systems e.g. outbreaks of group panic, "hysteria" and smothering, which result in mortality and economic losses.
3. Policy makers. Policy-makers in government and government agencies (e.g. Defra and Animal Health) responsible for producing Codes of Recommendations, inspecting farms and implementing animal welfare law already seek information in this area. For example, in 2005 Defra issued a call asking for research on whether mares should be slaughtered in sight of their foals. Without any fundamental knowledge in the area it was not possible to prepare an answer to this emotive issue.
4. Animal welfare organisations such as the RSPCA and Compassion in World Farming are extremely interested in the basic cognitive and emotional capacities of farm animals. CIWF, for example, devotes a substantial proportion of its webpages to questions of farm animal sentience see: http://www.ciwf.org.uk/animal_sentience/default.aspx. They constantly seek out and translate to a broader audience scientific evidence relating to farm animals' "intelligence and emotions". Their webpage even states that there is evidence that some animals "appear to show emotions similar to human empathy".
5. The public also has a seemingly insatiable demand for information about the intelligence and emotional lives of farm animals. We have been very actively involved in public engagement activities, giving well-received talks on "Farm Animal Minds" and "Animal Sentience", as well as contributing to programmes such as the BBC Secret Life of Farm Animals (2010) and the One Show (2011) which explored these capacities in chickens. This information informs the UK public and may guide their decisions about what types of animal products they wish to purchase, at what price. We have standing invitations from some media shows to contact them if we make interesting discoveries about chicken behaviour or cognition, and it would be our plan to do so as soon as we are sure we have robust results.

Publications

10 25 50
 
Description The work has been successful and has met the original objectives. The overall aim of the programme was to explore the foundational aspects of empathy in a bird species, the chicken. The work is of theoretical interest, as a comparative analysis of the evolution of empathy is as yet far from complete. It is also of practical interest as there are important animal welfare implications if animals are influenced by the emotional responses of their conspecifics.

Objective 1 was to assess the aversiveness of conspecific distress. We first confirmed that both adult hens and young chicks gave direct behavioural and physiological responses to an air puff stimulus and that both age-groups founds this stimulus mildly aversive. This was ascertained using both a conditioned place preference procedure and a runway test. We then used the conditioned place preference procedure to assess whether observer hens experienced a valenced reaction (one that was perceived either negatively or positively) when witnessing a conspecific receiving an air puff. Overall, despite our clear previous findings that mother hens are highly interested and aroused when witnessing air puffs to their chicks, we found that a valenced reaction was relatively mild and transitory. Thus, mother hens did preferentially choose a chamber where they had not previously witnessed mild chick distress over a chamber where mild chick distress had been observed. However, this preference declined rapidly. The functional reasons for this require further investigation - we propose that there may be a conflict between experiencing chick distress as aversive and being able to mount an effective pro-social (helping) response to remove chicks from danger. A paper on these findings has been submitted for publication.

Objective 2 examined whether an empathic response depends upon a shared initial emotional state between an adult observer and an adult conspecific. We conducted an experiment where observer hens were trained to locate an expected, fixed amount of food reward at the end of a runway. We then manipulated the amount of food available so that observer hens found more or less food than they were expecting - this should induce a more or less positive emotional state. These observer hens were then allowed to observe a conspecific bird also finding more or less food than expected. The heart rate and behavioural responses of the observers were recorded but the initial emotional state of the observers did not appear to greatly influence their reaction to the conspecific bird.

Objective 3 examined how observer hen expectation of personal safety or danger influenced her reactions and her pro-social (helping) behaviour towards her brood of chicks. Hens were initially trained that there were safe and dangerous areas of a large pen. In dangerous areas, a green light could signal the onset of an airpuff, whereas in safe areas the green light was not followed by any consequences. Hens trained that green light signalled a direct air puff to themselves, and hens trained that a green light signalled an air puff to their chicks, both gave more vocalisations and were able to lead chicks away from the dangerous area. Hens that had received the direct training were particularly vocal and more vigilant. Hens that had to rely on the responses of trained chicks showed a far lower response and reduced pro-social behaviour. This work confirms and builds on our previous finding that hens' empathic reactions are primarily based on their own knowledge and beliefs about a situation, with the chicks' behaviour having a lesser impact. A paper on this study is being prepared.

Objective 4 examined whether emotional transfer aided food aversion learning in adult observer hens. We assessed whether an observer's emotional reaction to the food disgust response of a conspecific was associated with the observer showing increased social avoidance of the same food items. There were no correlations between the extent of demonstrator disgust reaction or observer emotional response and the subsequent food choices of the observers. This line of research was closed.

Objective 5 was to determine whether stressful or otherwise aversive experiences can be reduced or 'buffered' by the presence of a conspecific - and further, to determine whether the degree of buffering is related to the empathic reaction of the conspecific. The interplay between emotional transfer and social buffering is likely to be an important factor in the escalation or de-escalation of arousal and distress in a social group. Pairs of chicks were exposed to an air puff treatment and a control, each with and without their mothers. Chicks showed a reliable suite of behavioural and physiological responses to the air puff, and these responses were ameliorated in the presence of the mother hen, showing that mothers do act as social buffers. However, not all mothers were equally effective - hens that had been more aroused by witnessing chick distress had a lower buffering capacity (Edgar et al., 2015a - listed in publications). We also found that chicks showed a reduced stress response when exposed to playback of maternal vocalisation from calm hens but no reduction in stress response in the presence of no playback, or playback from aroused hens (Edgar et al., 2015b -listed in publications).
The post-doctoral fellow employed on the grant successfully obtained a BBSRC fellowship in the final year of the project and has developed her own line of work, examining the commercial implications of simulating maternal care to improve the welfare of chickens. She has published a review of this general area of work which has been informed by the findings of this grant (Edgar et al., 2016 Animals 2016, 6(1), 2; doi:10.3390/ani6010002).
Sectors Agriculture, Food and Drink

 
Description The findings have been used in a variety of public engagement activities for a wide variety of audiences. Interest in the emotional and cognitive abilities of domestic animals remains very high, and we have contributed to many different media activities to inform this interest.
First Year Of Impact 2014
Sector Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

 
Description Workshop on use of thermography as animal welfare assessment tool.
Geographic Reach National 
Policy Influence Type Influenced training of practitioners or researchers
URL https://conferences.ncl.ac.uk/irtnewcastle2018/
 
Description Anniversary Future Leader Fellowship for Jo Edgar
Amount £292,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 03/2015 
End 02/2018
 
Description Independent contract with industry
Amount £88,000 (GBP)
Organisation Stonegate 
Sector Private
Country United Kingdom
Start 10/2015 
End 09/2018
 
Description International Partnering Awards
Amount £32,000 (GBP)
Funding ID BB/N021959/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start  
 
Description Research Grant - for Dr Jo Edgar
Amount £5,150 (GBP)
Organisation The Association for the Study of Animal Behaviour (ASAB) 
Sector Charity/Non Profit
Country Unknown
Start 04/2018 
End 07/2018
 
Description Collaboration and Visiting Researcher from University of Vienna 
Organisation University of Vienna
Country Austria 
Sector Academic/University 
PI Contribution Background work on emotional transfer and foundational empathic abilities in chickens. Developing tools and techniques for non-invasive recording of chicken emotion.
Collaborator Contribution Award obtained from Marietta Blau foundation for visiting researcher to come and run collaborative experiment.
Impact Outputs anticipated in 2019
Start Year 2018
 
Description Exhibition on animal emotion at the Natural History Museum of Neuchatel (Switzerland) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact We provided information and materials on our experiments on chicken empathy for an exhibition on animal emotion at the Natural History Museum of Neuchatel (Switzerland)

None, as yet
Year(s) Of Engagement Activity 2014
 
Description Invited seminar on empathy at Plymouth University 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Seminar to Biology department and undergraduate students on my work on empathy

No reported impacts
Year(s) Of Engagement Activity 2014
 
Description Public engagement event at the Bristol Neuroscience festival 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Adults and children were able to get involved with a task on measuring animal emotion and hear about what methods scientists use to measure emotion.

Children and young adults were interested in the BSc in Animal Behaviour and Welfare Science
Year(s) Of Engagement Activity 2014
 
Description Public engagement stand on 'Inside the chicken mind' 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact 462 visitors attended. The one-way system meant that is is likely that all of these visitors passed our stand on 'Inside the chicken mind'. The visitors were able to try out using a thermal imaging camera to use a task for measuring emotion in animals.

Exit polls were conducted by the Royal Veterinary College. These were completed by 80 groups of visitors and suggested that visitors learnt information on chicken behaviour and welfare that they didn't already know. At least 3 groups of visitors suggested that the event will change their egg buying habits.
Year(s) Of Engagement Activity 2012,2013,2014
 
Description Radio interview on German radio station, WDR 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Radio interview on German radio station, WDR on empathy in animals. This was broadcast nationally across Germany.

I received five email requests for further information from members of the public
Year(s) Of Engagement Activity 2014
 
Description Staff and Student talk at Anglia Ruskin University 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Undergraduate students
Results and Impact Dr Joanne Edgar invited to talk about maternal influences on chicken behaviour and welfare, including empathy work.
Year(s) Of Engagement Activity 2017
 
Description Webinar on empathy in animals for World Animal Protection 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I was one of two expert members of an online discussion as part of the World Animal Protection Sentience Debate on 'Can animals empathise and what does this mean for their welfare'. This involved answering questions from the panel and from the public on animal empathy.

No measurable impact to date.
Year(s) Of Engagement Activity 2015
URL http://www.animalmosaic.org/sentience/Debates/past-debates/default.aspx?page=0&debate=tcm:46-43176