Prepared by Professor Donald M. Broom and Dr Irene Rochlitz
Cambridge University Animal Welfare Information Service
Department of Veterinary Medicine
University of Cambridge
Madingley Road
Cambridge CB3 0ES, UK

Prepared by Professor Donald M. Broom and Dr Irene Rochlitz
Cambridge University Animal Welfare Information Service
Department of Veterinary Medicine
University of Cambridge
Madingley Road
Cambridge CB3 0ES, UK

University of Cambridge
CENTRE FOR ANIMAL WELFARE AND ANTHROZOOLOGYDEPARTMENT OF VETERINARY MEDICINEMADINGLEY ROADCAMBRIDGE CB3 0ES
UNITED KINGDOMThe Welfare of Ducks during Foie Gras Production
By Professor D.M. Broom and Dr. I. Rochlitz
Cambridge University Animal Welfare Information Service
14 September 2015
This review of the scientific literature on foie gras production in waterfowl focusses
on how the welfare of the birds may be affected by this farming practice. We
concentrate on the research on ducks rather than geese, because ducks are used inover 97 % of foie gras production in France (18,600 tons in 2013) (Litt and Pé 2015).
In 2012 Belgium produced approximately 25 tons of foie gras, 92% from ducks(Federale overheidsdienst 2014).
The large majority of publications in scientific journals on foie gras production comefrom researchers from INRA (Institut National de Recherches Agricoles) and fromITAVI (Institut Technique de l'Aviculture) in France, where there are centres
dedicated to this type of research. We are very grateful to Dr D. Guémené of INRA
and to Dr J. Litt of ITAVI, who provided us with references and were very helpful inanswering our questions.
Because of the limited amount of published peer-reviewed scientific literature on thewelfare of ducks during foie gras production, we have also consulted conference
proceedings, in particular proceedings from the biennial ‘Journées de la Recherche surles Palmipèdes à Foie Gras’, as well as technical brochures and stand-alone texts fromknown sources available on the internet. Wherever possible, we have tried to avoid
using material from groups advocating for or against the production of foie gras, andwe have avoided using unsubstantiated material from dubious sources or personal
opinion.
Campaigns against foie gras production have been led by a large number of animal
charities and organizations, some of which have prepared reports, documentaries andsimilar presentations on the subject which are available online. The charities include
the British Columbia SPCA, Compassion in World Farming, GAIA (Global Action in
the Interest of Animals), the Global Action Network, the Humane Society of theUnited States, L-214 Ethics and Animals, OneKind (formerly Advocates for2Animals), Viva!, World Animal Protection (formerly World Society for the Protectionof Animals), and others. There are concise reviews from the American Veterinary
Medical Association (JAVMA 2014) and the Canadian Veterinary Medical
Association (Skippon 2013). There are also many organizations that promote theproduction and consumption of foie gras.
The terms force-feeding or gavage are used interchangeably in this review. The mainfood used, maize, is usually called corn in North America. Other terms, such as
assisted feeding, cramming, and over-feeding, are sometimes used in the literature butmean the same as force-feeding or gavage. Much of the literature on foie gras
production is in French. In some instances, approximate translations have been usedbecause the equivalent word does not seem to exist in English (e.g. nervosisme,
peigne de contention).
We should like to thank the Belgian charity GAIA for supporting the preparation andwriting of this report at the University of Cambridge. The report focuses on theavailable scientific and other factual information and its content is independent offunding.

3

Table of Contents
Executive)Summary............................................................................................................................5)
Effects on health.............................................................................................................. 5)
Direct effects of force-feeding ........................................................................................ 6)
Housing ........................................................................................................................... 6)
Behaviour ........................................................................................................................ 7)
Other welfare considerations........................................................................................... 8)
Introduction...........................................................................................................................................9)
Health .................................................................................................................................................... 12
Mortality........................................................................................................................ 12)
Physical health .............................................................................................................. 12)
Liver steatosis................................................................................................................ 17)
Force<feeding ..................................................................................................................................... 20)
Behavioural responses................................................................................................... 20)
Physiological responses ................................................................................................ 24)
Thermal stress and panting............................................................................................ 25)
Production of foie gras without force-feeding .............................................................. 26)
Housing................................................................................................................................................. 29)
Housing in groups ......................................................................................................... 29)
Housing of foie gras ducks in Belgium......................................................................... 31)
Design of group cage to restrain ducks ......................................................................... 31)
Flooring and provision of litter ..................................................................................... 32)
Access to water ............................................................................................................. 33)
Behaviour ............................................................................................................................................ 36)
Nervousness and hyper-reactivity ................................................................................. 36)
Other)welfare)considerations ..................................................................................................... 39)
The human-animal relationship..................................................................................... 39)
Control over the environment and motivation .............................................................. 39)
The European Charter and the Welfare Quality® project............................................. 40)
Other stages of foie gras production ............................................................................. 41)
Conclusions......................................................................................................................................... 43)
Animal welfare-related.................................................................................................. 43)
General .......................................................................................................................... 45)
References........................................................................................................................................... 47)

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4

!
Executive Summary
This review of the scientific literature on foie gras production focuses on ducks andhow their welfare may be affected by this farming practice, in particular by forcefeeding. While the production of foie gras is recognised as being part of France’s long
gastronomic tradition it is worth noting that, historically, geese were used rather thanducks. In the past 10 years (2003 to 2013), national production has increased by
10.7%, with 97.6% coming from ducks. Current challenges to the sector in France
include the compulsory switch to group housing by January 2016, together with an
expectation of greater consideration of animal welfare by some consumers. The
switch to group housing has already occurred in Belgium.
With force-feeding the duck lacks control over an aspect of its life that is crucial to its
survival, the ingestion of appropriate quantities of an appropriate diet. This loss ofcontrol leads to very poor welfare.
Effects on health
Limited mortality figures are available for ducks used to produce foie gras. In 2013
the national average mortality was 2.2% (Litt and Pé 2015). SCAHAW (1998)
identified abnormalities in standing posture and gait, due to the enlarged fatty liverand other pathology such as bone fragility and foot lesions. More recently, Litt et aldescribed the development (2015a) and application (2015c) of an evaluation grid toassess the physical condition of mulard ducks. The condition of the birds deteriorated
as they passed through the successive stages of production. Wing damage, including
humeral fractures, was frequent and most likely to occur at the stages of collection,transport to the abattoir and shackling. Pododermatitis, hock burn, breast lesions, backinjury (most commonly scratches) and oesophagus (pseudo-crop) injuries wereidentified as useful measures to assess duck welfare.
There are studies comparing the extent of extravasation after nociceptive stimulation
with the force-feeding procedure, with evidence of oesophagitis in force-fed birds(Servière et al 2002, 2011). However, there are few data on post-mortem findings, at a
gross and microscopic level, of the upper digestive tract before, during and at the endof force-feeding. It seems that the likelihood of injury may be greater with group
housing because of the need to catch, position and restrain the birds.
The mulard duck is not migratory and never develops a greatly expanded liver whenreared normally. Yet by the end of the force-feeding period, its liver is 7 to 10 times
the size of a normal one with an average weight of 550 to 700 g and a fat content of
55.8%. Steatosis and other changes in the liver, as a result of feeding management forfoie gras production and force-feeding in particular, are pathological and can limit
duck survival. The reduction in the liver’s ability to detoxify, as indicated by a slower
BSP clearance, longer BSP half-life and raised liver enzymes at the end of the forcefeeding period, are all clear evidence of clinical pathology.

5Direct effects of force-feeding
Ducks show a range of behavioural responses to force-feeding, such as increased
agitation for the first 3 days, followed by increased periods of rest, wing-flapping andhead-shaking, less time with their head at rest, less grooming and preening behaviour
and reduced mobility. Due to the large amount of food that is force-fed, much of the
ducks’ time is spent panting in order to disperse the extra heat generated fromdigestion. This thermal stress makes them very prone to environmental heat stress,
which adds further to their discomfort. The description and interpretation of
behavioural changes around force-feeding from an animal welfare perspective islacking in many studies.
Faure et al (2001) compared the responses of force-fed ducks to the force-feeder with
their response to an unfamiliar person. The choice of response measure (flight
distance for a bird that is in a very small cage) and a confounding effect of thefamiliarity of the force-feeder make the conclusion that force-feeding is not aversive
to ducks scientifically invalid. Repeating this experiment using a better measure andtwo persons of equal familiarity, with one doing the force-feeding and the other not,could provide valid results.
There are studies of corticosterone and the HPA axis as indicators of stress in ducks
during force-feeding, but they vary greatly in experimental design. A complicating
factor is that food can suppress any increase in glucocorticoids and activity canincrease it. The results of Guémené et al (2001, 2006a) and Flament et al (2012) on
corticosterone levels before and after force-feeding are not in agreement with those of
Mirabito et al (2002c) and Mohammed et al (2014). We conclude that levels of bloodcorticosterone are a poor indicator of welfare in the studies reported on mulard ducks.
Attempts have been made to stimulate spontaneous over-eating in geese bymanipulating day length and feeding regimes, usually restriction followed by adlibitum feeding (Guy et al 2013). It seems that, under specific conditions of feeding
and photoperiod, geese are able to initiate spontaneous liver steatosis, offering thepossibility of foie gras production without the need to force-feed. However, thisalternative method currently has great negative impacts on the environment and someconsumers do not like the liver produced.
There may be a public health risk associated with foie gras consumption. Duck orgoose-derived foie gras contains amyloid protein, which could hasten thedevelopment of amyloidosis in a susceptible human population.
Housing
The keeping of ducks in cages scarcely larger than their bodies, and with the head andneck protruding so that force-feeding can occur, causes very poor welfare. After
January 2016 individual caging of ducks for foie gras production will be illegal inFrance, and should be replaced by group housing. Group housing has already been
implemented in Belgium. Group housing allows social interactions between birds and6gives them more space as a group. Compared with individual cages, group housing
leads to a decrease in liver weight, an increase in the time taken to perform the forcefeeding, and an increase in the amount of water used in cleaning. There is a slightincrease in the weight of the ‘magret’ (Litt 2010, Mirabito et al 2002a), an increase inliver defects at slaughter and fewer haematomas but more scratch lesions on the
carcasses.
Guémené et al (2002, 2006b) found that the capture and immobilisation of grouphoused birds for force-feeding can be a cause of repeated stress. A containment(restraint) method has been developed to overcome the problem of birds trying toescape, struggling or retreating to the back of the group cage and hence being difficult
to force-feed. Group-housed birds may be more susceptible to injury from handling,getting caught in the cage’s containment mechanism, or restrained for a long time.
Most cages are rather small, with a surface area per bird of 1200 cm2 to 1300 cm2 anda mesh floor made of steel or plastic. Despite Council of Europe (1999)
recommendations, neither litter, a resting place nor bedding material is provided. Thisis likely to lead to a worsening of contact dermatitis, which is already present at thestarter and grower stages of foie gras production (Litt et al 2015c), and also affectduck comfort, foraging and exploratory behaviours, and social interactions.
Ducks have a need for open water, for example in a trough or bath, to maintainplumage and body condition and to thermoregulate. It is legally required in many
countries that ducks should be able to fully immerse their head, to allow water tocover the head and be taken up by the beak so that they can shake water over theirbody without difficulty. Water troughs attached to the cages are provided for forcefed ducks. However, the minimum width and depth dimensions of troughs for thishave not been established, and to our knowledge there are no studies so far on troughuse or on water cleanliness and behaviours of force-fed ducks at the troughs. It also
seems that this facility is not always provided for ducks in the first two stages of foiegras production.
Behaviour
Mulard ducks are most often used for foie gras production, and some are recognised
as being particularly fearful, nervous and hyper-reactive – the term ‘nervosisme’ isused in French. They show panic and flight responses to the approach of humans andare generally described as being ‘sensitive to the environment’ (Guémené et al 2002,
Guémené et al 2006b, Laborde and Voisin 2013). In small individual cages, there
must be fear of humans in the ducks but, as they cannot move, it is not a problem forthe force-feeders. The move from individual to group housing seems to have brought
the problem of “nervosisme” in ducks to the fore. Mulards show obvious panic
responses and fear of humans, and appear to be more sensitive to social stress(isolation from other ducks) than the two parent types (Arnaud et al 2008). They also
have higher basal levels of corticosterone than parental lines.
Aspects of husbandry and management prior to force-feeding that may affect thebirds’ behaviours during force-feeding have been investigated by extensive
questionnaire and telephone surveys of force-feeders and duck farmers (Laborde andVoisin 2013). Reactive, nervous and fearful ducks clearly have poorer welfare thancalm ones, because they are less well able to cope with environmental changes and7with the presence of humans.
Other welfare considerations
There is substantial evidence that negative interactions between humans and animals
increase the animals’ fear and stress (Hemsworth 2007). In the case of foie gras
production, the relationship between the force-feeder and the force-fed ducks hasreceived little attention but the responses seen, such as struggling and escapebehaviours, are typical of farm animals subjected to routine procedures that they findpainful, frightening and unpleasant (Vinuela-Fernandez et al 2011).
The four welfare principles and 12 criteria proposed by the Welfare Quality® project(Blokhuis et al 2010) present general guidelines on the needs of animals and how they
may be met. Based on the information available to us, and contrary to the aspirationsof the European Federation of Foie Gras Charter, only three of the 12 criteria andnone of the welfare principles are met in current systems of foie gras production.
Ducks and geese in foie gras production are the only farmed animals that are notallowed to use their basic biological mechanisms to regulate their own food intake.
While the primary aim of this review has been to highlight the welfare problems in
the last stage of foie gras production, when ducks are force-fed, welfare problems
have also been identified in the first two stages, starter and growth. These include theearly, frequent and rapid development of footpad dermatitis, hock burns and breast
blisters, fear of humans and high sensitivity to the environment, and lack of access toopen water for bathing or at least full immersion of the head.

8

Introduction
In 1998, the Scientific Committee on Animal Health and Animal Welfare(SCAHAW) produced a report on the welfare aspects of foie gras production in ducks
and geese for the European Commission (SCAHAW 1998), and concluded that“force-feeding is detrimental to the welfare of the birds.” French researchers, who
studied several parameters during force-feeding and did not find scientific evidence tosupport the conclusion of SCAHAW, have objected to this conclusion (Guémené andGuy 2004).
The foie gras producing countries in the European Union are France, Belgium,
Bulgaria, Hungary and Spain (Litt and Pé 2015). A description of the background tofoie gras production in France can be found in Guémené and Guy (2004) and in
SCAHAW (1998). French law (French rural code L654-27-1) states that "Foie gras
belongs to the protected cultural and gastronomical heritage of France". However, thelong tradition in France was to use geese rather than ducks so the practice haschanged in a substantial way.
The European Federation of Foie Gras Producers was established in 2008 and has
members from the five European countries that produce foie gras. Their website
provides production data and seeks to uphold and defend the production of foie gras(see http://www.eurofoiegras.com/en/). Additional information on foie gras in
Belgium and Europe in general can be obtained from a recent Belgian scientific reportcommissioned by the Belgian Council on Animal Welfare (Federale overheidsdienst
2014). The two main areas of concern identified by the Belgian report are 1) whether
force-feeding is an ethical practice with regard to society’s obligations towards
animals and 2) the welfare of the force-fed ducks, especially when they become obese
towards the end of force-feeding.
We were unable to find reliable information for production methods in other EU
countries such as Spain, Bulgaria and Hungary; some is presented in SCAHAW(1998) but is likely to be out-of-date.
Some general data are presented below:• Approximately 25,000 tonnes of foie gras were produced in the EU in 2014
(23,000 tonnes of duck foie gras and 2,000 tonnes of goose foie gras).
• The sector generates more than 50,000 jobs in the EU, with a turnover of 4
billion euros.
• The EU produces approximately 90% of the world’s foie gras. The other main
producing countries are China, the United States and Canada.
• There were 13 producers of foie gras in Belgium in 2012, producing about 25
tons of foie gras every year from 50,000 ducks, which is approximately 0.09%
of global production (26,800 tons with 92% from ducks).
• Japan, Switzerland, Hong Kong and Israel are the main non-EU countries that
consume foie gras.
• The force-feeding of ducks and geese for the production of foie gras is bannedin a large number of European and other countries, but many countries where
production is banned continue to import it.

9The male mulard duck, the mulard duck being a hybrid between a muscovy drake(Cairina moschata) and a female domestic duck (Anas platyrhynchos), which is amallard, is used most frequently for force-feeding purposes because it has a goodpotential for production and is relatively easy to manage. The breed of domestic
duck/mallard most often used is the Pekin, so this name will be used here unlessspecified otherwise in a publication. Infertility problems in the production of thismulard hybrid have been mostly solved using artificial insemination.
The average weight of a foie gras liver produced in the male mulard duck is from 300
g to 560 g or more (Babilé et al 1996, Litt and Pé 2015). With such a large fatty liver,mortality rates increase so a focus of production companies is to reduce the durationof the force-feeding period (Guémené and Guy 2004). Producers have also
investigated the use of certain ingredients, added to the maize mash, which enhance
the response to force-feeding or improve the quality of the foie gras. In addition, there
is selection of parental strains for better carcass quality and for a body conformation
to produce larger breast muscle known as ‘magret’ (the breast meat of a mulard or
muscovy duck that has been force-fed to produce foie gras).
Producers have developed a specific feeding programme adapted to ducks, which isused prior to the force-feeding period and leads to a reduction in the duration of forcefeeding as compared with the duration when geese were used and when ducks werefirst used (Robin and Castaing 2002, Guémené et al 2007). It can be divided into threephases:1. Starting period: Birds are fed ad libitum from the time of hatching until 6 to 9
weeks. They are initially kept indoors, usually on straw as litter, and eventually
allowed outdoors during the day.
2. Growing period: Birds are feed-restricted for a period of 3 to 5 weeks. This
restriction may be in time (hourly feed restriction, when birds are fed ad-libitum but
for only a short period, once daily) or amount (quantitative feed restriction, whenbirds are fed a reduced amount of food daily).
Birds normally have outdoor access during the day.
3. Pre-force-feeding period: Birds are fed as much as possible for 3 to 10 days (hourlyor quantitative feed restriction may be used, but feeding increasing amounts). There isno defined crop in the mulard duck; an oesophageal ‘out-pouching’ is sometimes
called the pseudo-crop. This procedure before force-feeding has the aim of dilating
the oesophagus and stimulating the digestive secretions necessary for the assimilationof a large amount of food, and starting the process of liver steatosis. The liver canweigh up to 180 g by the end of this period, compared with 80 g normally.
Birds normally have outdoor access during the day.
The force-feeding procedure in ducks is described in SCAHAW (1998), Guémené andGuy (2004) and Guémené et al (2007). After about 12 weeks of age there is forced
daily ingestion, usually lasting 12 to 15 days, of increasing amounts of energy-richfood with a high carbohydrate, low protein content and an uneven amino acid andmineral balance (AVMA 2014). Ducks are force-fed twice daily; at the beginningeach receives 180 to 200 g of maize mash per meal, increasing to 450 g per meal
towards the end of the force-feeding period.
They are kept indoors in cages and in a controlled environment.
10Litt and Pé (2015) reviewed developments in the foie gras market and in farms
involved in the production of foie gras in France, collecting data from a range ofsources. In the past 10 years, national production has increased by 10.7%, from
17,217 tonnes in 2003 to 19,067 tonnes in 2013 with 97.6% coming from ducks.
Factors responsible for this production increase are said to be improved feed
conversion efficiency and a reduction in bird losses. This has occurred with ashortening of the force-feeding period to just over 12 days by 2013 (Litt and Pé 2015).
Nevertheless, profit margins have decreased as costs have increased. Current
challenges to the sector in France include the compulsory switch to group housing by
January 2016, together with an expectation of greater consideration of animal welfare
by consumers.
The normal behaviour, functioning and husbandry of ducks is described in Rodenburg
et al (2005), and of ducks and geese in SCAHAW (1998). Foie gras production ingeese is described in detail in SCAHAW (1998), FAO (2002) and Arroyo et al (2012).
The welfare of ducks in European duck husbandry systems is reviewed in Rodenburg
et al (2005), focusing on Pekin, muscovy and mulard duck genotypes used for meatand foie gras production. Factors that can affect duck welfare, such as stocking
density and group size, slatted, wire-mesh or straw-based flooring, lighting (intensityand duration), access to an outdoor run, and the provision of open water for drinking,bathing and swimming, are discussed. Welfare problems such as feather pecking andcannibalism, fear and stress, and diseases are assessed, and the various systems in use
in Europe are described. The review acknowledges that while giving ducks access to
straw, an outdoor run, or open water increases their behavioural opportunities(dabbling, foraging, preening, bathing, and swimming), this must be done in an
optimal way because it can lead to poor hygiene and increased risks to health andfood safety. Good practical solutions have to allow the expression of natural
behaviours but not lead to, or at least minimize, hygiene or health problems. Specifichusbandry features that affect the welfare of the mulard duck in foie gras production
are identified in the review as:
•
•
•
•
•
•

fear reactions to humans
high stocking density
no access to water for bathing
no access to bedding
use of slatted or wire mesh floors
the force-feeding procedure itself and the consequent liver steatosis.

These concerns are broadly in agreement with the main aspects of welfare associatedwith foie gras production that we have identified in this review. We have chosen toaddress these in five broad categories: health problems (physical and liver steatosis),force-feeding, housing, behaviour problems, and other welfare considerations. We
finish with a list of animal welfare-related and general conclusions. An executive
summary is presented on page 5.

11

HealthMortality
Published data on the effects of force-feeding on duck health, and hence on a key
aspect of duck welfare, are lacking (Servière et al 2011). Limited mortality figures areavailable for ducks used to produce foie gras and it is difficult to find a reasonablebaseline for comparison, such as the mortality rate of non force-fed mulard ducks.
SCAHAW (1998) concluded that mortality during the force-feeding period was
typically 2 to 4%. The Institut Technique de l'Aviculture (ITAVI, Technical Instituteof Poultry Farming) reports a figure of 2 to 5%, in 2006 the national average mortalityof force-fed birds was 2.4% (Laborde et al 2010) and in 2013 it was 2.2% (Litt and Pé
2015).
In an experimental study which explored the effects of group size and stocking
density on a number of production measures, the mortality of ducks kept in groups of3, 6 or 9 and at stocking densities of 1000, 1500 and 2000 cm2 per bird ranged from
1.4% to 13.9%, with the highest mortality seen in the largest group with the highest
stocking density (9 ducks with 1000 cm2 floor space each). The average mortality was
5.6% (Mirabito et al 2002a). These data compare unfavourably with mortality rates ofmuscovy ducks in fattening units for meat production, where in the two weeks before
slaughter the mortality rate was 0.2% (SCAHAW 1998). On farms in the UK,
mortality rates were 5.2% for Pekin ducks reared to an average 3.35 kg at 48 days
(Jones and Dawkins 2010a) and less than 5% in a commercial trial evaluating open
water sources for farmed ducks over 43 days (Liste et al 2012). Most mortality inducks reared for meat would occur in the youngest birds but even if mortality ratevaried in a linear way with age, the expected rate for 12 days of 5.2% over 48 days
would be 1.3%.
Anecdotal observations by members of the European Scientific Committee on Animal
Health and Welfare (SCAHAW 1998) suggest that fattened ducks demonstrateabnormalities in standing posture and gait. This has occurred to the extent thatmortalities have been attributed to some ducks becoming immobile and therefore
unable to access water.
Physical health
The health of birds can be measured using a wide range of variables including bodyanatomy, posture, walking ability and gait, face, body and plumage condition,
presence and severity of visible skin lesions (footpad, toe and hock dermatitis, breast
lesions) as well as mortality (Jones and Dawkins 2010a, Liste et al 2012). Thesevariables inform us of the animals’ welfare and also of management procedures. For
example, the condition of the face, i.e. cleanliness of the nostrils, eyes and feathers,
informs about whether or not the duck is able to immerse its head fully under waterand keep its face clean. The presence of facial injuries provides information about thephysical damage done during the force-feeding procedure.
Ducks that are being force-fed large quantities of food demonstrate abnormalities instanding posture and gait, due to the enlarged liver and other pathology such as bone

12

fragility and foot lesions. The abnormal mineral balance in the diet that force-fed
birds receive is thought to lead to bone pathology which is compounded by the bird’s
weight and limited opportunities to build bone and muscle strength. Typically, bone
fractures occur on wing bones, mainly the humerus, and the prevalence of bone
fractures due to handling at slaughter is between 30 and 70% (SCAHAW 1998).
Other factors will also increase susceptibility to injury and distress during transport,such as fear of humans, obesity and substantially higher thermoregulatory demands
than those for normal ducks.
There are few studies of the effects of force-feeding on gross body anatomy.
SCAHAW (1998) observed, on visits to fattening units, that the legs of the force-fed
animals were pushed outwards, away from the midline of the body so that they met
the ground considerably further apart than is normal. The leg could not be held
vertically when the bird was standing or walking, and they concluded that this wascaused by the great expansion of the liver. They observed that the consequence wasthat birds with expanded livers had difficulty in standing and their natural gait andability to walk were severely impaired. They assumed that there must be increased
lateral force on the leg joints when birds with hypertrophied livers are standing or
walking but this has not been studied.
The use of individual cages, in which the birds cannot stand in a normal standing
position or walk, occurs in some countries but is expected to decline in France
following a change in the law. Individual caging has already been banned in Belgium.
These cages make it difficult to recognise leg problems and leg pain. In the study by
Carrière et al (2006b) on the behaviour of force-fed ducks kept in groups, the ducks
spent more time lying down and walked less frequently and for a shorter time thancontrol ducks (non force-fed but kept in the same conditions). The reasons for thiswere ascribed to the birds’ increased weight, but the mechanisms by which increased
weight led to reduced activity were not explored. It is possible that the excessive force
on leg joints caused pain, which led to a reduced inclination to walk. In addition,
hypertrophied livers can cause discomfort in a number of other species so somediscomfort may have resulted directly from the enlarged liver in force-fed birds(SCAHAW 1998). Measures such as posture and walking ability (gait) are commonlyused in the assessment of welfare of ducks (Jones and Dawkins 2010a, Liste et al2012).
Recently, Litt et al described the development (2015a) and application (2015c) of anevaluation grid (‘grille d’évaluation’) to assess the physical condition of mulard
ducks. The grid was applied to 63 groups of ducks on 44 different commercial farms
at the end of the three main stages of production: starter, grower and gavage(‘fattening’). Birds in the gavage group were evaluated after slaughter in an abattoir.
Different indicators were used for the different stages; for example, cleanliness at theend of the starter phase, feathering at the end of growth and pseudo-crop lesions at theend of gavage.
The average condition of the birds deteriorated as they passed through the successive
stages of production. Four physical abnormalities were noted at all three stages:dermatitis of the footpad, toe (digit) and hock (hock burn), and damage (degree offeathering or lesions) to the breast area (anterior sternum). Some lesions, such as
those caused by dermatitis of the footpad and toe, appeared very early on in the
production process and were present very frequently. However, they did not seem toworsen during gavage.

13

Lesions on the breastbone could be extensive and frequent by the end of gavage,
especially in winter. Ventral loss of feathering was also commonly noted, especiallyduring the growth stage. Wing damage was observed at slaughter. It was judged that88% of wing lesions were recent and probably occurred at the stages of collection,transport to the abattoir and shackling. Other body injuries, such as scratches to thedorsal part of the body, pseudo-crop injury and joint abnormalities, were noted afterslaughter. Overall, the prevalence of lesions varied greatly between farms and groupsof birds, and associations with fixed factors such as starter density and season were
not sufficient to explain this variability.
The study did not provide figures on the prevalence of lesions at each stage. What isclear, however, is that the welfare of the birds, as assessed by general condition,
deteriorated significantly as they progressed through the production stages. The
authors recommend that pododermatitis, hock burn, breast lesions, back injury (mostcommonly scratches) and pseudo-crop injuries are useful measures that should form
part of an evaluation grid to assess the welfare of the mulard duck during the threestages of production.
Contact dermatitis is an umbrella term that includes footpad and toe dermatitis (alsoknown as pododermatitis or foot burn), hock burns and breast blisters in poultry(Shepherd and Fairchild 2010, Hepworth et al 2011). Hock burns and breast blisters
are thought to be manifestations of the same condition that results in pododermatitis(Shepherd and Fairchild 2010). Lesions can vary in size and depth (Bassett 2009, Littet al 2015b) and scales for the grading of their severity have been developed (Haslam
et al 2007, Bassett 2009, Litt et al 2015b). Pododermatitis lesions are characterised byinflammation and necrosis, ranging from superficial to deep, on the plantar surface ofthe footpads and toes (Shepherd and Fairchild 2010). Deep ulcers may lead toabscesses and thickening of underlying tissues and structures (Greene et al 1985).
Hock burns and breast blisters are not usually associated with bacterial infections.
Sudden changes in intestinal flora when ducks are force-fed can lead to gastrointestinal upset and diarrhoea. An increase in total flora load and in faecal streptococci
has been noted in the first stages of force-feeding. Enteric flora overgrowth andinfections may exacerbate any existing footpad and breast dermatitis and blisters, andbe a cause of mortality in force-fed birds (Laborde et al 2010).
Contact dermatitis causes significant economic loss and is also a cause of pain,
disability and poor welfare. The condition is painful because of the associated tissue
trauma (Haslam et al 2007). Animal welfare audits often use pododermatitis, hockburn and breast lesions as indicators of housing conditions and bird welfare (Haslam
et al 2007, Hepworth et al 2011).
In a survey of Pekin ducks commercially reared for meat in the UK, the physical andplumage condition of the ducks was recorded at two ages, 23 and 41 days (Jones andDawkins 2010a). This included eye, nostril and feather state, posture, walking ability,feather cleanliness, footpad dermatitis, callous toe and stubbly quill (short broken
feathers on the breast). At 23 days, more than 98% of inspected ducks were scored ashaving clean eyes, nostrils and feathers and almost 98% walked upright, althoughwalking ability was variable. At 41 days approximately 84% and 67% of ducks hadclean eyes and feathers and 98% clean nostrils with over 94% having an upright
posture. The birds’ condition deteriorated between 23 and 41 days, but this was notmarked. At slaughter, the incidence of moderate and severe footpad dermatitis lesions
was 10% and 3%, 32% of ducks had calloused toes and 11% had pink hocks. Contact
dermatitis lesions were mild and general condition good in other commercial trials
14

evaluating open water sources for farmed ducks over 43 days (O’Driscoll and Broom
2011, Liste et al 2012).
The frequency of poor welfare associated with such health problems in ducks reared
for foie gras production is much higher than that described above for ducks reared formeat production. Litt et al (2015b) found that by 14 weeks of age, the end of gavage,
all duck foot samples had moderate to marked signs of epidermal ulceration, visible tothe naked eye. Very severe ulcerative lesions, sometimes with secondary pustular
infections, were noted in some birds. From the recent published data on force-fed
ducks, it seems that pododermatitis is common, develops early in their lifetime andworsens with age. Biija et al (2013) studied ducks during the period prior to gavage,
when they were allowed outdoor access either onto a meadow with scattered trees oronto woodland. At 9 and 11 weeks of age, both groups had developed moderate tosevere pododermatitis, especially the group with woodland access.
There are some limitations in comparing birds kept in different systems. While forcefed ducks are similar to ducks kept for normal meat production in that they are fastgrowing, reach heavy bodyweights and often have reduced mobility at the end stagesof production, force-fed ducks are kept for longer, gain proportionally much moreweight, and are housed, managed and fed differently. Ducks confined in small
individual cages are not able to walk so walking difficulties might not be noticed. The
recent studies, and the creation of an evaluation grid, are the first steps towards thedevelopment of an evidence-based welfare assessment protocol for force-fed ducks.
The assessment of animal welfare is performed, wherever possible, using a wide
range of indicators such as the animal’s health, physiological state, behaviour andmental state (Broom and Fraser 2015). The study by Litt et al (2015c) gives us an
insight into what the animal is feeling, as contact dermatitis lesions are painful(Haslam et al 2007). Further studies are needed, in particular those that focus on the
animals’ physical condition and behaviour during gavage. However, in view of theearly appearance of contact dermatitis lesions and the general deterioration of theanimals’ body condition, the earlier production stages (starter and grower) should also
be examined. Finally, the high proportion (88%) of recent wing lesions that probably
occurred at the stages of collection, transport to the abattoir and shackling also causevery poor welfare and should be studied and prevented.
Reports of post-mortem examinations of ducks that die during or at the end of theforce-feeding period are sparse in the scientific literature. In general, there isinsufficient information on injuries and death due to force-feeding, on the incidenceof secondary infections of the oesophagus (such as Candidiasis, a yeast infection due
to Candida albicans) and on other complications that may arise. SCAHAW (1998)
report that, in one study, secondary infections with C.albicans were present in up to
6% of birds. In an internet presentation on the mulard duck used for foie gras
production Guérin (2015), a French veterinary surgeon from the École Nationale
Vétérinaire, Toulouse, lists the main causes of illness and death during the forcefeeding period. The main illnesses are respiratory and ocular disease, locomotor
disorders (loss of balance, myositis), digestive disorders (oesophagitis, candidiasis,
enteritis) and focal necrosis of the liver. Causes of death at the beginning of gavage
include cholera (Vibrio cholerae) and at the end include respiratory insufficiency anddisease, enteric disorders, cardiac myopathy and other causes such as cloacitis, ascites
and liver haemorrhages.
15

The act of gavage, where a rigid tube is inserted into the upper digestive tract, clearly
has the potential to be painful if performed rapidly or without due care. Therefore, thecondition of the oesophagus and pseudo-crop before, during and at the end of forcefeeding is of particular interest. A number of studies have looked for histologicalevidence of pain in ducks at different stages of the force-feeding period. Servière et al(2002) describes signs of sub-acute moderate and multifocal oesophagitis in force-fed
birds. Inflammatory foci may develop as a result of effects of abrasion and distension
caused by the boluses of food on tissues of the upper digestive tract. In anotherexperiment, ducks that were force-fed were compared with pharmacologically treatedcontrol ducks, in which necrosis of the oesophagus was provoked under anaesthesia
by an irritating substance containing mustard oil. Local inflammatory processes
resulting in focal extravasation responses, revealed by a specific marker, were very
severe in control ducks, but were not observed in force-fed ducks at the beginning or
the middle of the force-feeding period. However, areas of extravasation wereobserved in a few ducks by the end of force-feeding and were probably due tomoderate inflammation. Observations of peripheral and central neuronal activation
showed indications of pain signaling in the brain and spinal cord of chemically treatedbirds, and low level signaling in force-fed ducks (Servière et al 2002).
More recently, further experiments similar to the one described above were carriedout, but hydrochloric acid (HCl) was used instead of mustard oil as an irritatingchemical substance to induce neurogenic inflammation of the upper digestive tract(Servière et al 2011). Four regions of the upper digestive tract were examined, and in
the case of force-fed ducks, four different feeding periods as well. The authors
conclude that compared with extravasation after chemical nociceptive stimulation, themechanical insult to the oesophageal walls, potentially associated with the‘preparation for force-feeding’ phase and with the force-feeding procedure, ismoderate. The question remains whether mechanical stimulation, such as excessive
distension, induces visceral nociception.
While there are studies comparing the extent of extravasation after nociceptive
stimulation with the force-feeding procedure, there is a lack of data on post-mortem
findings, at a gross and microscopic level, of the upper digestive tract before, during
and at the end of force-feeding. Descriptive studies of the injuries, the incidence of
secondary infections of the upper digestive tract, and information on othercomplications that may occur as a result of force-feeding, such as injuries and lesions
on the face and eyes, are needed. This is particularly urgent as it seems that thelikelihood of injury may be greater with group housing because of the need to catch,
position and restrain the birds.

16

Liver steatosis
Some migratory waterfowl, such as greylag geese Anser anser, the same species as
the domestic goose, eat more than the normal amount of food in the days before
migration. The muscovy and the mulard duck are non-migratory and most populationsof wild mallard migrate little. Unlike the greylag goose, traditionally the main species
used for foie gras production, the mulard duck and its two parental species never havea greatly expanded liver when reared normally. Force-feeding results in an increase inliver size and fat content. By the end of the force-feeding period, the duck’s liver is 7
to 10 times the size of a normal liver with an average weight of 550 to 700 g and a fat
content of 55.8%. This increase in liver weight is accompanied by a substantial
overall live-weight gain in the range of 50 to 85%. In comparison, the average weightof a liver of a non force-fed drake is 76 g with a fat content of 6.6% (Babilé et al1996).
Steatosis and other changes that are caused in the liver, as a result of generalmanagement for foie gras production and force-feeding in particular, are pathologicaland can limit the survival potential of the ducks. The enlarged liver may compress
airsacs, reducing respiratory capacity, and other abdominal organs and where liverfunction is severely compromised hepatic encephalopathy (central nervous
dysfunction due to effects of toxins such as ammonia on the brain) may develop(SCAHAW 1998, Broom and Fraser 2015).
Steatosis develops because of the accumulation of triglycerides in hepatocytes (liver
cells); a detailed illustration of the process is presented in Baéza et al (2013). Maize,
consisting mainly of starch and low in fat and protein, is fed in large amounts. This
stimulates two transcription factors regulated by insulin, SREBP-1c, and by glucose,
ChREBP, which promote glycolysis and lipogenesis. Fatty liver results essentiallyfrom an increased capacity of hepatic lipogenesis, an insufficient hepatic capacity toexport newly synthesised triglycerides, and a limited capacity of peripheral tissues totake up circulating lipids, thus favouring their return towards the liver. There is failureof the liver to release fat into the blood, hypertrophy of hepatocytes which accumulate
fat together with other components (water, minerals, proteins, phospholipids), anddecreased retention of essential fatty acids.
The synthesis of lipids in the liver is maximised when the food fed during gavage ishigh in starch and low in protein. To reduce the ducks’ capacity to make Very Low
Density Lipoprotein (VLDL), which carries lipids away from the hepatocytes toperipheral tissue, the diet is restricted in levels of certain nutrients necessary for theirsynthesis such as the amino acids methionine and choline (Gabarrou et al 1996).
Maize has high levels of thiamine and biotin, which are necessary for the conversion
of sugars to lipids. Force-feeding a high-energy, high carbohydrate diet turns a normalliver (weighing 69 g) into a fatty one (695 g) in under two weeks (Gabarrou et al1996). The potential to develop hepatic steatosis depends on the species of waterfowl
and also varies with the genotype (Baéza et al 2013).
In an experiment by Babilé et al (1996), mulard ducks were force-fed for 10, 13 and16 days, and at the end of each force-feeding period were released back into the rearer(grower) group. For the first few days they did not eat but drank copiously. The
longer the force-feeding period, the longer it took for ducks to start eating again (8 to
15 days). They lost a lot of weight in the first week. The liver returned to its initial17

weight after 15 days following the end of force-feeding for groups force-fed for 10
and 13 days, and took 30 days to return to initial weight for those force-fed for 16
days. These results give an insight into the degree of insult from which the liver had
to recover. Prolonging the force-feeding from 13 to 16 days has a disproportional
effect on time to weight recovery (from 15 to 30 days), suggesting that 16 days offorce-feeding brings the duck close to severe liver dysfunction and failure.
Bénard et al (2006) examined the effects of force-feeding on liver function,
morphology and pathology. Ducks were force-fed for 2 weeks and then received
normal ad-libitum feeding for 4 weeks. This cycle was performed 3 times, with forcefed birds compared with a control group fed ad-libitum throughout. Birds were kept ingroups, and blood samples were taken at the end of every force-feeding or freefeeding cycle for the test birds and at the same time in the controls. A
bromosulphophthalein (BSP) clearance test, a measure of the liver’s ability todetoxify, was also performed. Birds were killed after 2, 6, 8, 12, 14 and 18 weeks andtheir livers examined.
While the weight of the non force-fed birds did not change significantly, the ducks
that were force-fed put on weight (1.5 to 2 kg), but lost it during the 4 week nonforce-feeding period (1.4 to 2.3 kg). Gross hepatomegaly was noted in force-fed birds.
Concentrations of liver enzymes lipase, alanine aminotransferase and aspartate
aminotransferase rose significantly at the end of each force-feeding period, and after 4
weeks of normal feeding, returned to levels similar to those of the control group. In
control birds after 2 weeks, hepatocytes had an average diameter of 7-10 µm whereas
signs of steatosis were obvious in force-fed birds: hepatocyte diameter was 35-40 µm
and the cell was full of fat vacuoles. After 3 cycles of force-feeding the liver structure
was similar but 4 weeks later, most of the liver cells had an average diameter of 7-15
µm, similar to that of controls, and were no longer full of fat. BSP clearance, as
measured by the area under the curve, was reduced in force-fed birds at 2 and 8
weeks, compared with controls, while it returned to normal after periods of freefeeding as well as after the third force-feeding cycle. The elimination half-life (T½) of
BSP was greatly prolonged at the end of each force-feeding period but returned tonormal (values same as controls) after 4 weeks of free feeding.
The force-fed birds were kept on wire mesh floors and developed signs of tibio-tarsal
arthritis as well as skin calluses on their feet; these lesions disappeared when birds
were returned to straw litter for free feeding.
The authors conclude that, since animals were able to withstand three consecutive
cycles of force-feeding, with four-week intervals of normal feeding, and that nopathology was found after these rest periods, force-feeding does not induce dietrelated pathological changes as the steatosis is reversible, and therefore animal
welfare is not adversely affected. However, survival after a problem does not meanthat there was no problem. The reduction in the liver’s ability to detoxify, as indicatedby a slower BSP clearance, longer BSP half-life and raised liver enzymes (due tohepatocyte cell membrane damage allowing the enzymes to enter the blood), at theend of the force-feeding period, are all clear evidence of clinical pathology. This andvarious other data (SCAHAW 1998) show that the liver steatosis obtained by forcefeeding induces an impairment of hepatic function, as demonstrated frommorphometric, biochemical, histological and pharmacological aspects. While this wasreversible in the studies described above, the reversibility of steatosis does not meanthat the changes in the liver are not pathological. In the Babilé et al (1996) study, liver
weight after 16 days of force-feeding took 30 days to reduce to normal, and in otherstudies the mortality of ducks increases when the force-feeding period is prolonged
18

beyond a period of 15 days (SCAHAW 1998). The cause of death is likely to be liver
failure or its consequences such as necrosis and haemorrhage, septicaemia or
respiratory disease, enteric disorders, cardiac myopathy and other causes (Guérin2015).
There are other points made in the article by Bénard et al (1996) that require
discussion. The force-feeding was performed on ducks housed in groups on the floor,
and force-fed by one person seated on a stool within the pen. This force-feeding is not
typical of current practice (Litt et al 2010), taking much longer, about 30 seconds. The
birds were closely examined twice daily throughout the study, and after an initial 3day period of agitation showed increasingly longer periods of rest between each forcefeeding, as well as an increase in wing flapping. These behavioural changes are notexplained. Increasingly longer periods of rest could be due to lethargy or abdominal
discomfort, agitation and wing flapping due to pain, distress or fear. There is no
mention of whether there was access to water troughs for head immersion and wet
preening, and despite close examination twice daily, there is no description of thecondition of the ducks, in particular of their face, eyes and nostrils (indicators of water
access for head immersion, or site for injury). The findings of this study do notsupport the authors’ conclusion that the force-feeding did not cause any suffering.
Carrière et al (2006a) adopted a different biochemical approach to evaluate thefunctional state of the liver, by looking for markers of liver inflammation and ofsteatosis. Peroxysome Proliferator-Activated Receptor (PPAR) is a protein receptor
found within the cell nucleus; PPARs are active as transcription factors which control
the expression of genes involved in cellular metabolism. There are three subtypes ofthese ligand-activated transcription factors (α, β/δ and γ); α and γ have important rolesin the liver and in fatty tissue. PPARγ is involved in the control of lipid metabolism,
stimulates adipocyte differentiation and is implicated in the development of theinflammatory process. PPARγ tends to have an anti-inflammatory effect.
This study looked at the expression of PPARγ during the development of liver
steatosis in mulard ducks. This protein was present at a basal level in the liver andwas over-expressed during force-feeding, and even more so at the end of forcefeeding. The authors conclude that there is a need to determine whether or not there isexpression of different sub-types of PPARγs, and if this expression is associated withthe development of a non-pathological liver steatosis or of an inflammatory liver
steatitis resulting from the feeding of a high-energy diet. We have not foundadditional published data on PPARs in ducks undergoing force-feeding.
Baéza et al (2013) suggest that few signs of liver inflammation develop during forcefeeding because birds lack some cytokines which are secreted by the fatty tissue ofmammals, such as TNF-α, and which are pro-inflammatory in some liver conditions
in humans. However, it seems that TNF homologues do exist in birds (Varfolomeev
and Ashkenazi 2004) so it would be worthwhile to examine their action in forcefeeding.
We suggest that other physiological measures that could be used in the assessment ofliver function in force-fed ducks include bile acids, ammonia, urea nitrogen, gamma
glutamyltransferase, uric acid and coagulation factors (for example fibrinogen) in the
blood and ketones in the blood or urine (Harr 2005). These measures are commonlyused in other species. Because maize is not a balanced diet for ducks, otherabnormalities may be present such as hormone imbalances or altered calcium tophosphate ratios leading to bone pathology (SCAHAW 1998).
19Force-feeding
A major objection to the practice of foie gras production is to the consequences offorcing food into the animals. The animal no longer has autonomy when it comes towhat, when and how much it will eat. It is not allowed to feed spontaneously or showa food preference, and is force-fed increasingly large amounts of food, all of which
are much greater than it would normally eat. The diet itself is formulated for
maximum growth and fat deposition, especially in the liver but also subcutaneously as‘magret’. The insertion of a feeding tube to deliver the ration, in most cases in an
automated manner, has the potential to cause injury to the animal’s bill, face, neckand upper digestive tract. Birds used in foie gras production are the only farmed
species that is not allowed to feed by expressing normal feeding behaviour.
Ducks are fed considerably more during the force-feeding period than they would eat
voluntarily, and they receive this food without having the possibility to forage in a
species-specific manner. Each duck will be motivated to perform normal foraging
activities, such as searching for food, pecking, nibbling, dabbling, up-ending andswallowing, even if it is force-fed. Such a need to forage for food is not met duringforce-feeding (SCAHAW 1998).
Several behavioural characteristics of mulard ducks can be recognised. On the one
hand they are fearful of humans and nervous, or ‘sensitive to the environment’(Laborde and Voisin 2013), while on the other hand they are gregarious and sociabletowards conspecifics (Guémené et al 2006b). While the last two characteristics
indicate that group-housing is likely to be enriching, the first two make mulard ducks
particularly unsuitable for force-feeding because, fearful of humans and nervous, theystruggle, try to escape or retreat to the back of the cage.
Behavioural responses
Compared with physical and physiological effects, there is an even greater lack ofpublished data on the behavioural responses to force-feeding, both during theprocedure itself and at other times, for example immediately beforehand when the
ducks anticipate a potentially unpleasant experience, and afterwards when the duckhas to assimilate a large amount of food that has been forcibly inserted into its
oesophagus. When behavioural responses are described, their interpretation andsignificance from a welfare perspective is sometimes lacking or incomplete.
The gag or pharyngeal reflex is a reflex contraction of the back of the throat, evoked
by touching the roof of the mouth, the back of the tongue, the area around the tonsils
or the back of the throat. There is a contraction of both sides of the posterior oral andpharyngeal musculature, and humans report that this is an unpleasant experience (seehttp://www.neuroanatomy.wisc.edu/virtualbrain/BrainStem/09NA.html).
The reflex helps to prevent material from entering the throat, except as part of normal
swallowing, and protects against choking and aspiration. Some people have ahypersensitive reflex while others can learn to inhibit it (for example, sword
swallowers).

20

There is controversy as to whether the reflex is present in ducks; we agree withSCAHAW (1998) that it is. Unlike some birds such as pelicans and storks, mulard
ducks consume food by dabbling and sieving and do not swallow large food items.
There is no reason why the pharyngeal reflex would be absent in these ducks.
Initially, force-feeding stimulates this reflex but after a certain time it stops. The
adaptation time required for the gag reflex to be extinguished, and how the duck isaffected by this, are not known. For example, some birds shake their head vigorously
after force-feeding but the specific cause of this is not known (Carrière et al 2006b).
Head-shaking is normally an indicator of an aversive event and is also noted whenbirds are deprived of access to open water (Rodenburg et al 2005).
The behaviour of mulard ducks following force-feeding, during the hour after thesecond, twelfth and twenty-fourth meal (three time periods), was compared withmulard ducks that were kept in the same conditions but not handled or force-fed(Carrière et al 2006b). The ducks were not kept in typical production cages, as they
were group-housed in cages (3 ducks per cage with 80 cm X 80 cm floor surfacearea). These cages were large enough to allow birds to stretch and spread their wings,
so they could show a wider range of behaviours than ducks kept in standard individual
cages. The test birds were force-fed twice daily for 13 days (the amount fed at eachmeal, and whether the amount increased day by day, are not specified). The control
ducks had ad-libitum access to food, which was provided every morning at the sametime as the test ducks were force-fed. The behaviour of the control ducks was videorecorded the day after the recording of the test ducks.
The force-fed ducks spent more time lying down, and walked less frequently and for ashorter time than control ducks. There was a trend towards spending less ‘time
standing immobile’, and an interaction with time period for the behaviours ‘time spent
standing immobile’ and ‘time spent lying’. The authors explain these results by thephysical effects of the ducks’ weight gain on posture and movement; birds gain a lotof weight during the force-feeding period and their mobility is greatly reduced. We
argue that this has consequences with regard to the ducks’ welfare. The excess weight(caused by force-feeding) can reduce the animal’s mobility by a number of
mechanisms including pressure from an enlarged liver on limbs, reduced respiratory
capability and pain. Lack of mobility is likely to lead to further consequences that
reduce welfare such as poor muscle strength, bone fractures, skin lesions and alteredsocial interactions with conspecifics. When birds are kept in restrictive environments
where they cannot move freely, recognising mobility problems becomes difficult.
Over the force-feeding period, the test birds spent less time with their head at rest
while this behaviour in control birds did not diminish over the same period. After thetwenty-fourth meal, hardly any time was spent with the head in the rest position. Thismay have resulted from the animal’s excess weight, from food in the oesophagus orfrom discomfort in the head and neck region and would prevent the bird from resting
fully.
Grooming and preening behaviour occurred less often, and for a shorter time, in theforce-fed birds (evident from the first time period). After the last time period, forcefed birds spread their wings less and over time they shook their tail less frequently
than controls. There was a trend for the force-fed birds to groom their conspecifics
less than controls and for this behaviour to decrease over time, suggesting a decreasein social interactions. However, there was no evidence of increased aggression
between force-fed ducks.
Most intensive farms for foie gras production have air ventilation systems to keep
ambient temperatures relatively low, in an attempt to reduce thermal stress in the21birds. Nevertheless, the force-fed ducks spent a lot of time panting. This behaviour
was not evident in the control ducks at any time, and not in test ducks after the second
meal. After the twelfth meal 5 out of 9 ducks panted, and after the twenty-fourth all
panted in the hour after force-feeding. Panting to aid evaporative cooling is part of thethermoregulatory response to the ingestion of large amounts of high-energy food, as isimmersion of the face and, by wet preening, the body in water. The birds had accessto water but it is not clear whether the access was to water troughs, showers, baths ornipple drinkers; it seems that water was only available for drinking. The test birds hadto spend a significant proportion of their time in behaviour to restore thermal
homeostasis that was disrupted as a result of force-feeding, something the control
birds fed ad-libitum did not have to do. In addition, the apparent lack of adequate
access to water, which would have helped them cope with this disruption, further
reduced their welfare.
Force-fed birds shook their head more than controls, especially after the first force-fed
meal but also after subsequent meals. The authors suggest that this may be a reaction
to handling by the force-feeder, or to the introduction of a large amount of food into
the oesophagus. Head-shaking is also seen when birds are deprived of access to open
water (Rodenburg et al 2005), and may be evidence of stimulation of the gag reflex(see above). Self-grooming, preening and wing-stretching are all behaviours generally
associated with good welfare in birds (Rodenburg et al 2005). The time spent
performing these behaviours was less in force-fed compared with control birds anddecreased over time, further evidence for poor welfare in force-fed birds.
This study was limited to examining the behaviour of birds for one hour after forcefeeding; examination of further time periods during the day would have been useful.
In addition, there may have been an effect of handling, separate from the effect offorce-feeding, on the behaviour of the test birds but this was not explored as controls
were not handled prior to feeding.
For comparison, the time budget of commercially-reared Pekin ducks at 41 days was:
1.5% of the time feeding, 6.7% drinking, 4.2% rooting and 15.5% dry preening (Jonesand Dawkins 2010b). They spent 43.5% of time fairly inactive, either remaining
stationary but alert, resting, settling to rest or panting (12% of time, and 6% at 23days). Most of the rest of the time (17%) they performed comfort behaviours such asleg, wing or head stretches and shaking their body, wing flapping, wing lifting, andsmall mandibular movements. On average 4.6% of their time was spent walking and1.8% wet preening.
The behavioural responses to force-feeding were also examined in ducks by Faure etal (1998, 2001). Two types of experiment were performed. In the first, ducks weretrained to be fed in a pen 8 m away from their rearing pen and were then force-fed in
the same feeding pen. The hypothesis was that if force-feeding caused aversion, theanimals would not spontaneously leave their rearing pen or go into the test pen.
At 11 weeks of age ducks were kept in 8 groups of 15 until the end of the experiment.
During the 14-day training period, they were trained to go spontaneously, once a day(in the morning), from the rearing pen to the test pen where they received their daily
food ration (200 g of cooked maize). During the first 3 days of training, theexperimenter pushed out the ducks. After this initial training period, whenever the
ducks did not move spontaneously after the door opened, the observer entered the pen
after an interval of 30 s and pushed the ducks towards the door. The same procedure
was repeated if the ducks did not enter the test pen within the required interval of 30 s.
After all the food had been eaten (60 to 90 min), the door of the test pen was opened
and the same procedure repeated. After two weeks of training to go spontaneously
22

from the rearing to the test pen, where they received their daily meal, the control
group followed the same procedure whereas the test group received the same quantity(200 g) of cooked maize by force-feeding for a period of 10 days.
During the test period, control animals spontaneously left the rearing pen in about halfof the tests, whereas none of the force-fed groups did. The control groups also
spontaneously entered the test pen during each test, whereas only about a half of theforce-fed groups did. These results indicate that the ducks found the force-feeding
procedure aversive and were reluctant to enter the pen where they were force-fed.
Some problems were encountered with the training of the birds because on days 13
and 14 the usual experimenter was absent and was replaced by an unfamiliar person,
which produced a level of avoidance comparable to the force-feeding itself.
It is not clear why the amount of food fed to the ducks throughout the 10 day
experimental period stayed the same and was given just once daily, as in thecommercial situation the amount of food force-fed to the ducks would increase fromday to day, and would be given twice daily. Force-fed ducks normally receive 250 g
of food on the first day, rising to 900 g by the tenth day (Guémené et al 2007).
Feeding increasing amounts of food, and force-feeding twice daily, is likely toincrease the strength of aversion shown to force-feeding.
In this force-feeding study in which aversion responses were recorded, the ducks were
subjected to possible positive and negative stimuli simultaneously and the net effectmeasured. The occasion during the day when feeding occurred was likely to bepositive and the procedures of force-feeding were likely to have negative components.
It may also be that any aversion responses tended to have negative consequences so
the birds learned not to show them.
In the second experiment by Faure et al (2001), the flight distances of ducks from theperson who performed the force-feeding and from an unknown observer were
measured for ducks housed in individual cages. Flight distance was the distance
between the person and the duck’s cage, at the time when the duck withdrew its head
into the cage as the person approached it. Tests were performed 2 to 6 hours after theforce-fed meal on days 3, 7, 9 and 11.
On day 3 the flight distances were similar. On day 7 and day 9 ducks avoided theunknown person more than the force-feeder and their avoidance of the force-feeder
decreased during the force-feeding period. The authors conclude that there was noevidence of an aversion for the person who performed the force-feeding.
However, examination of the graph provided shows that the avoidance of theunfamiliar person decreased after day 7 at a greater rate than for the force-feeder, andwas not greater than for the force-feeder by day 11. It is possible that the decrease inflight distance for the force-feeder between days 3 and 7 was an effect of familiarity
rather than evidence of a lack of aversion, because the force-feeder would have beenfeeding the birds on days 4, 5 and 6, when the approach test did not take place and thebirds were not exposed to the unfamiliar person. However, after days 7 and 9 theunfamiliar person would now be a familiar non force-feeder so the flight distancedecreased even more rapidly than for the force-feeder, suggesting that, with both
persons now considered familiar, there was aversion to the force-feeder because flight
distance between days 9 and 11 decreased more slowly for the force-feeder than for
the non force-feeder. Repeating this experiment using two persons of equalfamiliarity, with one doing the force-feeding and the other not, would be useful. Since
the birds were confined to individual cages with no space to escape or hide, the rangeof aversion behaviours the ducks could show was very limited. Withdrawal of thehead into the cage as a person approached may not be the best measure of aversion,
especially when it is used as the sole measure. In fact such a response could cause
23greater problems for the bird. Withdrawal of the head when the person wants to put
the tube in the oesophagus could lead to rough handling or other punitive actions by
the person feeding. Another result of head withdrawal that would be negative for the
duck could be that the process lasted longer. Ducks could learn not to withdraw theirheads for either of these reasons. Hence this is a poorly-controlled experiment withalternative explanations for the results. It does not demonstrate that force-feeding is
not aversive to ducks.

Physiological responses
Guémené et al (2001) examined the effects of the force-feeding procedure and its
different components (handling, intubation) on various physiological indicators of
acute and chronic stress in male mulard ducks before and during a 12-day forcefeeding period. The highest concentration of corticosterone were measured after
injection of an ACTH agonist, during the pre-experimental period when the ducks
were still housed in group floor pens, and at the time of transfer from pens to
individual cages. The group housed ducks had to be caught before being sampled,which is likely to have caused stress and raised corticosterone levels. During theforce-feeding period, corticosterone measured before and after force-feeding did notincrease significantly although there was a non-significant trend towards an increaseon some days. The different components of force-feeding, including handling andintubation, force-feeding with a standard or a large amount of food had no significant
effect upon corticosterone concentrations. There was no indication from ACTH
agonist challenge either of a change in adrenal sensitivity or a change in its
responsiveness. The authors conclude that there was no significant indication thatforce-feeding was perceived as an acute or chronic stress by male mulard ducks, inthe experimental conditions. They acknowledge, however, that it remains to be shownthat the ducks’ adrenocorticotrophic axis is responsive to acute stressors.
There were additional results that indicate that further research in this area is required.
For example, very high corticosterone concentrations were observed for all
experimental groups while the ducks were still in group pens and not yet force-fed.
There was a significant decrease in bodyweight for control, handled and intubatedducks over the 2 week period, which may have been the consequence of being housed
in individual cages. The heterocyte-lymphocyte ratio (sometimes a measure of morechronic stress) measured before and at the end of the force-feeding period did not
differ significantly, although there was a trend for the ratios to increase withincreasing physical handling (from controls to intubation to mild and full forcefeeding). The results of Guémené et al (2001) regarding corticosterone levels before
and after force-feeding are not in agreement with those of Mirabito et al (2002c).
Guémené et al (2001) found that corticosterone measured before and after forcefeeding did not increase significantly though there was a non-significant trend
towards an increase on some days. However, Mirabito et al (2002c) found that forcefeeding caused significant increases in corticosterone in some groups of ducks onsome days.
Another study by Guémené et al (2006a) sought to investigate further the HPA axis
functionality in male mulard ducks and to examine for possible interactions between
force-feeding practice and rearing environment on behavioural and physiologicalindicators of stress and poor welfare. This publication is complex, and consists of24

three separate experiments: the first two measured plasma corticosterone levels andthe third studied behaviour patterns. In the first experiment, birds were kept inindividual cages and half were force-fed while half were not. Within each group somebirds were subjected to further treatment, being placed on the floor and tightly
constrained in a net for 10 minutes after force-feeding, either on the 8th and 13th day
or twice daily throughout the experimental period. In the second experiment, threehousing environments were compared: slatted floor group pens, group cages andindividual cages. In the third experiment, ducks were kept in three housing
environments (as described in experiment 2) and their behaviour recorded.
The results of the first two experiments confirmed those from previous studies(Guémené et al 2001). When in individual cages the majority of male mulard ducks
did not respond by a significant increase in corticosterone levels after force-feeding,even on its first occurrence. Force-fed and non force-fed ducks were, however,sensitive to physical treatments such as a tight constraint in a net. The response tophysical treatments reduced with time, which may have indicated habituation. For
birds kept in group pens or cages, the capture and immobilisation before force-feeding
may have been a cause of repeated stress.
Flament et al (2012) also found that corticosterone levels in force-fed ducks did notincrease during the force-feeding period. However, triglyceride and aspartate
aminotransferase (AST) levels in plasma increased during force-feeding and untilslaughter, as did levels of uric acid in plasma. The authors explain raised uric acidlevels as being most likely due to the oxidative stress associated with force-feeding.
In contrast, in a recent study on force-feeding and stress in muscovy ducks bloodcorticosterone levels of force-fed ducks rose while those of controls did not and ducks
that were force-fed spent more time panting than controls (Mohammed et al 2014). It
is not clear whether a lighting schedule of 23 hours light and 1 hour darkness wasused; this schedule may affect the ducks’ behaviour and physiology.
A complicating factor in the interpretation of the results of Guémené and others is thatthe birds were receiving food and this can suppress any increase in glucocorticoids. A
further factor is that the birds had previous experience of being force-fed and arelikely to have learned that the increased activity, associated with greater plasma
corticosterone concentration, is counter-productive. A bird which shows an excited
response is more likely to be hurt by the force-feeding process. Hence, any birds
which can suppress such a response are likely to have less pain and other poor welfare
than birds that react actively. In the same way, human prisoners who showed apassive response when at risk of being caused pain, survived better than those whoreacted.
In summary, from the studies presented above we can conclude that levels of bloodcorticosterone are a poor indicator of welfare in mulard ducks (JAVMA 2014). They
must be considered in conjunction with other welfare indicators such as health,pathology, other physiological measures, behaviour and other indicators of mental
state (Broom and Johnson 2000).
Thermal stress and panting
Due to the large amount of food that is force-fed, ducks are susceptible to thermal
25stress which causes panting in order to disperse the extra heat generated fromdigestion. Force-fed birds may spend large amounts of time, standing or lying down,
performing this behaviour and unable to do anything else (like preening or resting).
This thermal stress makes the duck very prone to environmental heat stress, whichadds further to their discomfort, reduces food digestibility and increases mortality.
Nutritional supplements containing electrolytes and anti-oxidants have beendeveloped to mitigate these effects (Mathiaud et al 2013).
Immersion in water is another homeostatic mechanism for thermoregulation in birds.
If water for immersion is not available then heat stress becomes a risk (Rodenburg etal 2005) (see Housing).
Production of foie gras without force-feeding
Researchers are keen to find a way of producing foie gras without the need to forcefeed (Guy et al 2007). The aim is to stimulate ducks and geese to over-eat voluntarily
to a degree that is sufficient to lead to hepatic steatosis. The options they present are:
1. Manipulating feeding behaviour
Over-eating can be stimulated by previous restriction followed by ad-libitum
provision of food, and is affected by photoperiod and other climaticconditions. It is not a long-lasting effect and results are variable.
2. Surgery
Methods to destroy the satiety centre in the brain of geese have given varying
results. For ethical reasons this approach is unacceptable.
3. Pharmacological
It may be possible to induce transient over-eating by passive or active
immunization against the hormone leptin, which regulates appetite. There haseven been a study looking at the use of the compound arsenic to induce fatty
liver in mule ducks (Chen and Chiout 2001). These un-natural processes areunlikely to be acceptable to the consumer.
4. Genetics
It may be possible to select for individuals that over-eat. However, it is likelythat the birds will fatten excessively and this would have a negative effect on
reproductive success of the parents.
5. Other
A completely different approach would be firstly to interfere with Very Low
Density Lipoprotein transport of newly synthesized lipids from the liver toperipheral tissues and, secondly, to limit the storage of lipids in peripheral
tissues (Guy et al 2007). However, methods to do this have not beendeveloped.
Attempts have been made to stimulate spontaneous over-eating in geese bymanipulating day length and feeding regimes (usually restriction followed by adlibitum feeding) (Fernandez et al 2013, Guy et al 2013, Bonnefont et al 2015,
Fernandez et al 2015). In a study by Guy et al (2013), male Greylag Landaise geese
were fed ad-libitum from birth to 5 weeks of age, and then were food-restricted until
20 weeks when they were again fed ad-libitum until death. The diet from 20 weeks
onwards consisted of maize. Photoperiod is a major environmental factor controlling
migration and the pre-migratory fattening process in birds. From 21 to 23 weeks, thedaylight duration was progressively reduced from 10 to 7 h and kept at 7 h until the26end of the experiment (week 31). Thirty birds were slaughtered at 19, 23, 25, 27, 29,
and 31 weeks. During the first 2 weeks after maize delivery, the average consumptionrose up to 600 g/bird/d and decreased slowly thereafter to reach 270 g at week 31.
Liver weight increased from 95 g (week 19) to 514 g (week 31), and most of thesechanges were due to the increase in lipid content from 6 to 50% of liver weight. There
was no mortality during the experimental period. Histology indicated that fat
accumulated in the hepatocytes, which increased in size without any sign ofinflammation or degeneration. It seems that, under specific conditions of photoperiod
and feeding, geese are able to initiate spontaneous liver steatosis. However, thevariability in the response was high; at week 31, the coefficient of variation for liver
weight was 45%.
In a similar experiment by Bonnefont et al (2015), a high mortality rate (20%) was
noted in geese between 133 (19 weeks) and 217 days (31 weeks) on ad-libitum
feeding. This was most likely due to the very early and rapid development of liver
steatosis. There was also a great variation in response. In another study, when feeding
was restricted and then allowed ad-libitum for longer, Fernandez et al (2013) notedthat geese kept in individual cages ate 13% less food than those kept in groups,
underlining the importance of social interactions on food intake. In this study, theperiod of feeding was prolonged but performance did not improve; in fact, geese
started dying after 32 weeks.
These experiments indicate that, in certain conditions, geese are able to develop
hepatic steatosis without force-feeding, offering the possibility of foie gras productionin this species without the need to force-feed. However, these alternative methods
currently have negative impacts on the environment (Brachet et al 2015). Indicators ofenvironmental impact were estimated and were greater for non force-fed than forcefed geese. This was mainly due to a greater consumption of food despite lower liver
weights, longer production times, larger amounts of animal waste produced andoverall lower productivity. In addition, it seems that the liver produced by thesealternative methods is less liked by consumers (Fernandez et al 2015).
A farmer from Extremadura, Spain, produces foie gras from geese under the label‘Sousa & Labourdette’. These geese are free-range and feed freely on a range of foods
available on the farm. The product is described as ‘natural’ and ‘ethical’. It is
produced in small amounts at a high cost and is aimed at a niche market, particularly
restaurants (see http://www.sousa-labourdette.com/). The French company Labeyrie
makes products containing the liver and fat from ducks and geese that have not been
force-fed, called Foie Fin.
Faux Gras® by GAIA is a Belgian plant-based product that is sold in mostsupermarkets in Belgium during the Christmas and New Year period (seehttp://fauxgras.be/language-choice/). Faux Gras™ is an American product made of
toasted walnuts, lentils and onions and is marketed as a humane vegan alternative tofoie gras (see http://www.regalvegan.com/site/products/faux-gras/).
Risks of foie gras consumption to humans
There are concerns that the consumption of foie gras may have negative effects onhumans. Solomon et al (2007) found that duck- or goose-derived foie gras contained
amyloid protein and raised the possibility that this protein could hasten thedevelopment of amyloidosis in a susceptible population. Their abstract is as follows:
27

“The human cerebral and systemic amyloidoses and prion-associated spongiform
encephalopathies are acquired or inherited protein folding disorders in which
normally soluble proteins or peptides are converted into fibrillar aggregates. This is a
nucleation-dependent process that can be initiated or accelerated by fibril seeds
formed from homologous or heterologous amyloidogenic precursors that serve as an
amyloid enhancing factor (AEF), and has pathogenic significance in that disease may
be transmitted by oral ingestion or parenteral administration of these conformationallyaltered components. Except for infected brain tissue, specific dietary sources of AEF
have not been identified.
Here we report that commercially available duck- or goose-derived foie gras contains
bi-refringent congophilic fibrillar material composed of serum amyloid A-related
protein that acted as a potent AEF in a transgenic murine model of secondary(amyloid A protein) amyloidosis. When such mice were injected with or fed amyloid
extracted from foie gras, the animals developed extensive systemic pathologicaldeposits. These experimental data provide evidence that an amyloid-containing foodproduct hastened the development of amyloid protein A amyloidosis in a susceptible
population.
On this basis, we posit that this and perhaps other forms of amyloidosis may betransmissible, akin to the infectious nature of prion-related illnesses.”
A more recent publication (Greger 2008) has the following abstract:“The demonstration of oral Amyloid-A (AA) fibril transmissibility has raised foodsafety questions about the consumption of amyloidotic viscera. In a presumed prionlike mechanism, amyloid fibrils have been shown to trigger and accelerate thedevelopment of AA amyloidosis in rodent models.
The finding of amyloid fibrils in edible avian and mammalian food animal tissues,
combined with the inability of cooking temperatures to eliminate their amyloidogenic
potential, has led to concerns that products such as pâté de foie gras may activate areactive systemic amyloidosis in susceptible consumers.
Given the ability of amyloid fibrils to cross-seed the formation of chemicallyheterologous fibrils, the speculative etiologic role of dietary amyloid in other disease
processes involving amyloid formation such as Alzheimer’s disease and Type II
Diabetes is also discussed. “28Housing
Housing in groups
Until recently, the majority of production systems placed ducks in individual cages
during the force-feeding period rather than in group pens or cages. The main
advantages to the producer are that the ducks could be force-fed rapidly one after theother, without the feeder having to catch them, and that “they always remain in theright position” (Guémené and Guy 2004). Individual cages were small and greatly
restricted the bird’s movements; they did not allow the bird to turn around, stretch andflap its wings, stretch to its full vertical height or horizontal length or show more thana minimal behavioural repertoire. The degree of restriction increased as the bird grew
fatter during the force-feeding period. Using a pneumatic or hydraulic force-feeding
pipe, up to 400 individually caged ducks could be force-fed by one person per hour.
After January 2016, individual caging of ducks for foie gras production will be illegal
in France, and should be replaced by group (collective) housing. Ducks will have to
be housed in groups of at least 3 birds. The Council of Europe recommendations(1999) concerning Muscovy ducks (Cairina moschata) and hybrids of Muscovy anddomestic ducks (Anas platyrhynchos) state that housing systems for ducks shall allow
the birds to:
Article 10.7
- stand with a normal posture,- turn around without difficulty,- defaecate showing normal movements,- flap the wings,- show normal preening movements,- perform normal social interactions,- carry out normal feeding and drinking movements.
Group housing allows social interactions between birds and gives them more space asa group. The individual bird should be able to turn around and spread its wings fully,
and stretch vertically to its full height. Factors that affect welfare in group housing
include group size, stocking density, social interactions, type of flooring used, use oflitter or bedding material, access to water for drinking, and the provision of water forbathing, or at least full immersion of the head. Management of the air space andventilation, maintaining cleanliness and controlling disease, and ensuringhomogeneity of groups are also important. Potential undesirable effects of group
housing include increased aggression between birds, difficulty in maintaining
cleanliness (especially in larger groups), competition at water sources and increased
stress and fear when the birds are caught for force-feeding. Guémené et al (2002,
2006a) found that the capture and immobilisation of group-housed birds for forcefeeding can be a cause of repeated stress.
Due to the impending legislative change, over recent years research has focussed onalternatives to individual cages. Mirabito et al (2006) compared ducks kept in groups(from 3 to 8 per group) to those in individual cages. The study was done in twostages; in the first the group cages provided birds with a floor area of 2000 cm2 to29

2142 cm2 each, and in the second between 1500 cm2 and 1875 cm2 each. All 3 typesof group cage had a movable front wall device to restrain ducks (‘peigne decontention’) and two had a movable back wall. When the birds were slaughtered,variables such as mortality during the force-feeding period, final body weight,‘magret’, liver and thigh weight, lesions on the carcasses such as claw scratches andkeel injuries, thigh haematomas, fractures or fissures of the humeral head and generalcleanliness of the birds were recorded. The terms ‘smaller’ and ‘larger’ refer tosurface area per bird, and not to total group size unless specified.
Mortality in group cages was 6.2 % in the first stage, and 3.4 % in the second stage
when there were smaller cages with fewer ducks and better sanitary conditions. The
highest mortality occurred in the largest cage with the most ducks, in the first stage
where there were problems with maintaining cleanliness. In terms of performanceoutcomes, group housing (and surface area of 2000 cm2) had a positive effect on‘magret’ weight but not on other measures such as liver or body weight. For othervariables such as carcass lesions and general cleanliness, there were differences
between individual and group cages on the one hand, and within group cages on theother. Lesions on the back and scratches occurred more frequently in groups than in
individually housed ducks, as would be expected, whereas the opposite was true forhumeral head lesions, perhaps a reflection of reduced activity and subsequent bone
weakness.
Previous work on group housing has examined the effect of floor space and group sizeon production (mortality, liver weight, carcass and thigh weight, final body weight),
behaviour and blood corticosterone (Mirabito et al 2002a,b,c). In general, the bestproduction results were obtained when ducks had 2000 cm2 of floor area each, andlarger groups (9 ducks) had higher mortality and poorer cleanliness (Mirabito et al
2002a). However, birds kept at the highest stocking density in the smallest group had
more humeral lesions at slaughter, perhaps again a reflection of reduced activity andsubsequent bone weakness. Surface area per bird was the main factor that influenced
behaviour, with birds kept at 1000 cm2 each moving less and stretching their wings
less frequently than birds kept at 1500 or 2000 cm2 density (Mirabito et al 2002b). For
the latter behaviour, there appeared to be an interaction between group size andstocking density, as frequency of wing-stretching was affected by the total amount of
space available.
The effects of group size (3, 6 or 9 ducks) and surface area per bird (1000, 1500 and2000 cm2) on blood corticosterone before and after force-feeding and on the HPA axis
was explored, and compared with birds housed individually (Mirabito et al 2002c).
There was great variability in resting corticosterone levels, and force-feeding caused
significant increases in corticosterone in some groups on some days, so it was notpossible to draw meaningful conclusions regarding the effects of different housing
conditions on blood levels of corticosterone. Increases were noted for ducks housed
individually after the 1st and 11th meal, findings which are not in agreement with thoseof Guémené et al (2001). There was no evidence of abnormalities in sensitivity orreactivity of the HPA axis, except for some unusual results obtained for the group of 6
ducks kept at 1500 cm2 stocking density.
Between 2007 and 2009, trials of group versus individual housing of ducks were
performed by Litt (2010). One model of group housing was compared with twomodels of individual housing, using the following criteria: product quality (liver and‘magret’), the condition of the carcass immediately after slaughter, work conditions

30

for the force-feeder and the use of water for cleaning. The focus was largely on
production outcomes rather than on welfare.
While birds were fed the same amount, group housing led to a decrease in liver
weight (-77 g on average), an increase of 55% in the time taken to perform the forcefeeding (from 5.6 seconds to 8.7 seconds per bird), and a 34% increase in the amountof water used in cleaning (although this figure has been reduced in more recent
models). There was a slight increase in the weight of the ‘magret’ (+ 4 g), a finding
also noted by Mirabito et al (2002a). In group-housed birds there was also an increasein liver defects at slaughter (+15%) and fewer haematomas but more scratch lesions
on the carcasses; there were more scratches on the thighs than on the back. Breast
lesions were more severe and more frequent when birds were kept on a plastic rather
than a steel mesh floor.
More recent models of group housing have been modified, particularly with regard to
the containment (restraint) of birds and the work conditions of force-feeders during
feeding and cleaning.
Housing of foie gras ducks in Belgium
In a Royal Decree of December 2010, Belgium adopted modifications to the Royal
Decree of April 1994 (which arose from legislation of August 1986 regarding thewelfare and protection of animals, article 36,10). These forbid the use of individual
cages, require group housing with at least three birds per cage or housing in larger
groups. They have been implemented throughout Belgium and individual caging does
not occur.
The recommendations state, for example, that the period of force-feeding in ducks
must not last longer than 14 days, and that the water troughs should allow birds toimmerse their head (dimensions are given: at least 75 mm deep and 65 mm wide).
There should be no fewer than three ducks per cage, with each having at least 1200
cm2 of surface area. With larger groups, there should be no more than six ducks per
m2. There is no mention of the provision of litter or bedding material, or the use of a
restraint method during force-feeding. In general, the recommendations are largely
based on the existing French scientific literature, what is practised in France, and EU
guidelines.
At the end of 2012 force-feeding of ducks was practised in 11 farms in Wallonia andone in Flanders (Marlier and Bauwens 2012). Six used group cages and six kept
groups in pens on the floor (‘parc collectif’). Litter was provided in four of them,while two had a wire mesh floor. Usually litter consisted of whole wheat straw added
twice daily during feeding time. This litter would provide some degree ofenrichment, by creating a more comfortable floor surface and as substratum for
manipulation and exploration.
Foie gras production in Belgium is regulated and controlled by the public authorities(see http://www.eurofoiegras.com/en/page/initiatives_p139/). The Belgian Federal
Agency for the Safety of the Food Chain (AFSCA) certifies production sites.
Design of group cage to restrain ducks
A containment (restraint) method has been developed by researchers and producers, toovercome the problem of birds trying to escape, struggling or retreating to the back of
the group cage and hence being difficult to force-feed. A movable back wall pushes
31the birds towards the front. As the birds collect at the front, the front vertical walldescends back over them (‘peigne de contention’) and prevents them escaping or
moving much (see http://www.eyhartzea.com for an illustration; on this farm with thissystem, approximately 100 birds can be force-fed in under 20 minutes).
Group-housed birds may be more susceptible to injury from handling, getting caught
in the cage’s containment mechanism, or restrained in an uncomfortable position for along time, (up to 30 minutes) as the force-feeder works up one row of cages and backdown the other before releasing the containment mechanism. Because birds
immobilised by the movable grids may be facing any direction, the force-feeder must
be able to insert the feeding tube from any angle (Cepso 2013). There is likely toincrease the risk of injury to the bird’s face, upper digestive tract or body, especially if
it struggles and resists or if other birds get in the way. This makes it more difficult,and takes longer, for the force-feeder to carry out their task, especially with larger
groups (Mirabito et al 2002a, Litt 2010). The force-feeder is unable to develop a
steady rhythm, working their way uninterrupted along a row of cages as was possible
with individual caging, and this further increases the risk of injury to the birds.
The brochure by the agricultural group Cepso Chambagri “Le logement collectif pourle gavage des canards”, produced in 2013, illustrates 12 different types of cages andprovides a summary table which compares all the cage systems with regard to density,
floor space per bird, and other parameters (Cepso 2013). Ten out of 12 cages cancontain between 4 and 6 birds with the remaining 2 having a capacity of up to 10
birds. Recommended cage floor surface area is 4000 cm2 for 3 ducks, 5000 cm2 for 4
and at least 1200 cm2 surface area per bird (the equivalent of 2 size A4 sheets ofpaper), for 5 ducks or more. The cage should be tall enough for the bird to stretch
fully to its vertical height; there is no roof. Ten of the systems have a movable backwall, and all but one have a front vertical wall that can move back and down to
restrain the birds (‘peigne de contention’). Based on available published studies, thechoice of cage floor surface area per bird seems to be a compromise between
economics (1000-1200 cm2) and duck comfort (1500-2000 cm2). Most are on thesmaller side, with a surface area per bird of 1200 cm2 to 1300 cm2. To our knowledge,
there are no published studies on the social interactions between birds, optimal groupsize, behaviour time budgets or approaches to improve the cage environment.
Flooring and provision of litter
Force-fed ducks are usually kept on a mesh floor (‘caillebotis’) made of some type ofsteel (galvanised or stainless) and less commonly of plastic. They gain weight very
quickly and their liver expands, which causes problems with mobility due toexcessive weight on joints and loss of balance (SCAHAW 1998). They become
inactive and spend more time resting on a bare surface, as litter is not provided. Thissequence of events is likely to lead to a worsening of contact dermatitis (footpad,
hock and breast lesions), which is already present at the starter and grower stages offoie gras production (Litt et al 2015c). Conditions during these stages are relevant to
the development and course of the disease. Contact dermatitis is common, develops
early during the production process, worsens with age and is a cause of pain anddisability. The reasons for this are not obvious; the condition is already of moderate tomarked severity when birds are ready for force-feeding. It is not clear whether lesions
improve, worsen (Litt et al 2015b) or stay the same (Litt et al 2015a,c) during force32

feeding. Bénard et al (2006) noted that force-fed birds kept on wire mesh floors
developed signs of tibio-tarsal arthritis as well as skin calluses on their feet. Theselesions disappeared when birds were returned to straw litter for free feeding.
Many environmental factors have been associated with the development of contact
dermatitis; why it occurs in some flocks and not in others is not fully understood. It is
recognised that a major contributing factor, particularly at the onset, is the type oflitter, or ground quality if litter is not provided. Damage occurs to the skin surfacesthat have prolonged contact with the litter, usually starting with the footpad and toes,
then the rear surface of the hock and, when severe, the breast area. While highmoisture litter is sufficient to cause the condition, litter depth, ammonia levels,
climatic conditions, condensation, ventilation, stocking density, rearing system, leg
weakness, ground quality and diet are also recognised as causative factors (Haslam etal 2007, Bassett 2009, Shepherd and Fairchild 2010, Hepworth et al 2011).
Methionine may be a contributing cause, and maize is methionine-deficient (Bassett2009). Imbalances in other amino acids (such as choline) and vitamins may also be
involved.
EU recommendations (Council of Europe 1999) concerning Muscovy ducks (Cairina
moschata) and hybrids of Muscovy and domestic ducks (Anas platyrhynchos) state:
Article 10
6. Where ducks are housed, floors shall be of a suitable design and material and notcause discomfort, distress or injury to the birds. The floor shall include an area
sufficient to enable all birds to rest simultaneously and covered with an appropriate
bedding material
Article 11
4. Adequate litter shall be provided and maintained, as far as possible, in a dry, friablestate in order to help the birds to keep themselves clean and to enrich the environment
Despite these recommendations, currently the standard group cage used for foie gras
production lacks an area where ducks can rest together, and there is no bedding
material or litter to ensure their comfort and cleanliness, and to provide substratum forforaging and exploratory behaviours. The cage is not enriched beyond the provisionof water troughs and of conspecifics. The floor consists of a relatively hard, baresurface which may worsen the birds’ condition, having already developed contact
dermatitis in previous stages of production. The group cage is relatively barren andhas not ‘addressed the animal welfare issue’ as suggested by some sources. In many
ways it resembles the conventional battery cage for laying hens, a design banned in
the EU since January 2012 on welfare grounds, one difference being that the ducks
cannot feed for themselves.
Access to water
Ducks spend considerable time performing complex preening behaviours (Rodenburg
et al 2005). After feeding followed by bathing, ducks carry out a variety of shaking
movements to remove water. Cleaning movements are used to remove foreign bodies
and an elaborate sequence is carried out to distribute oil on the feathers from the33uropygial gland above the tail. This is necessary for waterproofing and heat
regulation. Preening is often followed by sleeping for a short period, and the sequenceof feeding, bathing, preening and sleeping may be repeated a number of times during
the day. Important elements of bathing are the immersion of the head and wings, andshaking water from these over the body.
EU recommendations (Council of Europe 1999) concerning Muscovy ducks (Cairina
moschata) and hybrids of Muscovy and domestic ducks (Anas platyrhynchos) state:
Article 10
2. Access to an outside run and water for bathing is necessary for ducks, as water
birds, to fulfill their biological requirements. Where such access is not possible, theducks must be provided with water facilities sufficient in number and so designed toallow water to cover the head and be taken up by the beak so that the duck can shakewater over the body without difficulty. The ducks should be allowed to dip their heads
under water.
The provision of a good open water system such as troughs improves eye, nostril andfeather condition and reduces disease (Knierim et al 2004, Jones et al 2009, Jones andDawkins 2010a,b, O’Driscoll and Broom 2011, O’Driscoll and Broom 2012). Water
troughs must be wide enough and deep enough so that ducks can immerse and wet
their head fully. The trough should also be long enough so that there is no competition
between ducks for access, although it may not be necessary for all birds to bathe
simultaneously (Waitt et al 2009). The Cepso brochure “Le logement collectif pour legavage des canards’ (Cepso 2013) states that there should be at least 800 mm lengthof water trough per cage, but it is not clear if this is dependent on group size. In
addition, the width and depth dimensions of the troughs are not supplied. The
brochure shows some of the systems with the troughs located centrally with cage units
either side, and some have the troughs on the outside of the cage, on the same side as
the force-feeder. Ensuring water cleanliness may be difficult, especially when troughs
are on the periphery of the cage, on the same side as the force-feeder. Also, birds may
be hesitant to approach this side because of its association with the force-feeder andwith being force-fed. If the troughs cannot be kept clean, a separate supply of water
for drinking purposes only (such as nipple drinkers) may be necessary (Liste et al2013, Broom and Fraser 2015).
While studies state that water troughs are provided for drinking and head immersion,
to our knowledge none published so far have examined whether the trough is actuallyused for what it is designed, or reported on water cleanliness and behaviours of forcefed ducks at the troughs. The troughs should be long, wide and deep enough to allow
the duck to immerse its head fully in water, but there is little information on the
optimal dimensions of water troughs. Dimensions are available for troughs used inexperimental conditions in British studies of farmed ducks, for example: 950 mm
long, 125 mm wide and 80 mm deep (Jones et al 2009, Waitt et al 2009) or 1600 mm
long, 150 mm wide and 100 mm deep (O’Driscoll and Broom 2011). However, ducks
in these studies are younger, smaller and lighter than ducks at force-feeding, and thetroughs would be placed on the ground rather than being attached to cages. A Belgianscientific report on foie gras production states legislation of 2010 that specifies theprovision of troughs that are at least 75 mm deep but only at least 65 mm wide
(Federale overheidsdienst 2014). Little attention seems to have been paid to water
trough dimensions in other studies, or to whether the birds are able to perform this34

immersive behaviour in addition to drinking, or to water cleanliness and maintenanceof troughs. As ducks lack sweat glands immersion in water, as well as panting, is avital homeostatic mechanism for thermoregulation. It is of paramount importance toforce-fed birds who are subjected to a high level of thermal stress due to the large
amounts of food fed.
In the past, force-fed mulard ducks kept in individual cages either had access to water
via nipple drinkers (Rodenburg et al 2005) or via troughs but, because of therestrictive cage, the type of trough and increasing bird size, they could not immerse
their heads in the water, spread water over their feathers and self-groom. They wereunable to keep their eyes, beaks, nostrils and feathers clean and photographs of forcefed ducks often showed them with dirty faces and necks, especially towards the end of
the force-feeding period. During force-feeding, which is a messy procedure, the maize
mash is likely to contaminate the bird, its cage and surroundings. It remains to be seen
whether group housing, with the provision of water facilities in the form of troughs,
results in cleaner, healthier birds with improved welfare.

35

Behaviour
Nervousness and hyper-reactivity
Mulard ducks are most often used for foie gras production, and are recognised as
being particularly fearful, nervous and hyper-reactive – the term ‘nervosisme’ is used
in French. They show panic and flight responses to the approach of humans and are
generally described as being ‘sensitive to the environment’ (Guémené et al 2002,
Guémené et al 2006b, Laborde and Voisin 2013). These behaviours become evident at
5 to 7 weeks of age. It seems that the move from individual to group housing hasbrought the problem of “nervosisme” in ducks to the fore.
French scientists have established a research project called “CaNervosisme” in an
attempt to address the undesirable behavioural characteristics of ‘nervosisme’. The
project includes a large number of different experiments looking at a range of features
such as the birds’ phenotype, genotype, genetic manipulations, rearing conditions,group size, behavioural and physiological responses and exposure to humans(Guémené et al 2002, Guémené et al 2004, Guémené et al 2006b).
Mulard ducks with white plumage are most often used for foie gras production, andare recognised as being particularly fearful, showing panic and flight responses to theapproach of humans and generally being highly reactive to their environment.
Guémené et al (2002) looked at the effects of genotype (2 strains A and B), phenotype(white, mostly white or coloured plumage) and early controlled exposure to humanson these responses.
Birds were kept in rearing pens until force-feeding 99 days later. Exposure to humans
consisted of walking through the group of animals for 5 mins three times a day (5days out of 7), and of individual handling once daily (5 days out of 7). Individual
handling involved collecting the animals at one end of their pen, catching them
individually and passing them to the other side of a barrier. The control groups
received the minimum amount of human handling necessary to carry out normal
husbandry procedures. Three behavioural tests (response to human approach in acorridor, response to a novel object or to a man in an arena, and an open field test)
were performed at 2 to 3 weeks and 9 to 10 weeks of age. After the birds weretransferred to individual cages for force-feeding, they were examined for their
response to the approach of the force-feeder on 4 occasions (after 3rd, 15th, 21st and25th meal, 2nd, 7th, 10th and 12th day). The birds’ reactions were scored as aggressive,
indifferent or fearful.
In general, plumage colour had no effect on behavioural responses, whereas genotype
and human handling did. Handling had a positive effect, independent of genotype or
phenotype, as birds were less likely to show escape responses to the approach ofhumans than non-handled birds. However, the results of the ‘response to the forcefeeder’ are less obvious; both handling and experimental group factors had asignificant effect on the birds’ behaviour on the first test occasion (3rd meal) but notthereafter. Within the handled groups, ducks of the B genotype with coloured
plumage were more indifferent, less aggressive and less frightened, whereas in the
non-handled group, ducks of the A genotype with white plumage were lessindifferent, more aggressive and more frightened. The authors raise the possibility
that the impression that ducks of white plumage are more fearful may be due to36

husbandry factors, because white ducks are more likely to be kept in large flocks inintensive production systems where contact with humans is minimal. Birds withcoloured plumage are more often found in smaller flocks where there is more humancontact. The lack of effect of previous handling on the response to the force-feeder,
except on the first test, suggests that aversion to the force-feeder or force-feeding
process over-rides the positive effect of handling.
Faure et al (2003) compared the susceptibility to fear and stress in two species andtheir hybrid. Male muscovy and male Pekin ducks and the male hybrid, the mulard,
were tested for fear and stress reactions using tonic immobility and fear of humans
behavioural tests. Blood was collected for corticosterone assay i) 10 minutes after the
tonic immobility test ii) before and after 10 minutes of restraint in a net, a treatmentthat has been shown to cause a significant increase in plasma corticosterone, and iii)
before and after the injection of 5 g/kg of synacthen (ACTH agonist).
The muscovy duck showed lower levels of fear reactions than the Pekin in the
majority of behavioural tests (six of eight). Corticosterone levels were also nearly
always the lowest in muscovy ducks (five of six tests). In general the muscovy duckappeared to be less fearful and less susceptible to hypothalamus-pituitaryadrenocortical (HPA) responses than the Pekin duck. The mulard was similar to one
parent or midway between the two for most tests but showed heterosis (a greater
response than the two parents) for fear of humans at 10 weeks of age. Corticosterone
levels in the mulard duck were midway between the two parents in most tests. The
best indication of the magnitude of the adrenal response is the increase incorticosterone in relation to basal and maximal concentrations, so comparisons ofactual increases in concentration across species give limited information.
In a more recent publication, Arnaud et al (2008) examined further the behaviouraland physiological fear responses in muscovy, Pekin and mulard ducks. Both parental
genotypes were very sensitive to stressors and highly fearful, especially to humanpresence or handling. However, they showed different behavioural responses: Pekinducks showed greater locomotor activity and panic behaviour, while muscovy ducks
showed greater avoidance. Hybrids showed greater panic responses and fear ofhumans, and appeared to be more sensitive to social stress (isolation from otherducks) than the two parent types, evidence of heterosis. A significant heterosis effect
was also found for basal adrenal activity, with mulard ducks having higher basal
levels of corticosterone than parental lines.
It has long been recognised by force-feeders that, in addition to genetics, theprovenance of the birds influences whether they are of the ‘calm’ or ‘nervous’ type.
Laborde and Voisin (2013) carried out extensive questionnaire and telephone surveys
of force-feeders and duck farmers, to explore aspects of husbandry and practice prior
to force-feeding that may affect the birds’ behaviours during force-feeding. Producers
were divided into two groups, those that produced ‘nervous’ and those that produced‘calm’ birds. Behavioural group did not affect production statistics such as mortality
or liver weight; effects were largely such that force-feeding was more difficult with‘nervous’ groups. Birds were described as agitated, retreating from the gavage tube,
causing wounds to conspecifics and the force-feeder, making the procedure last longer
and increasing the mental and physical strain on the force-feeder.
The husbandry and management of the birds prior to their entry into indoor housing,for the final 2-week period of force-feeding, was shown to affect their fearfulness
during force-feeding. Different aspects seemed to have positive, negative or no effects
37

although the differences between groups were not marked (P values are close to but
greater than 0.05; statistical methods are not described). Birds subjected to multiple
manipulations, for example weighing and vaccination, had a tendency to be lessnervous as did birds fed by manual rather than automated methods prior to forcefeeding. Birds reared on sandy soils, that experienced a rapid transfer to the forcefeeding site, or that came from remotely located farms, were more nervous.
This preliminary study has highlighted some of the many factors that may have aneffect on the subsequent behaviours of ducks during force-feeding. ‘Nervosisme’seems to have two main components: fear of humans and fear of the environment.
These two different kinds of fear are likely to have different aetiologies, paths ofdevelopment and influences and, therefore, require different remedial approaches.
Reactive, nervous and fearful ducks clearly have poorer welfare than calm ones,
because they are less well able to cope with environmental changes and with thepresence of humans. This has particularly severe effects on welfare for these birds
because the foie gras production process involves sudden environmental changes andclose human contact. For example, ducks are moved to the outdoors at the end of thestarter period and then suddenly brought indoors to an unfamiliar environment forforce-feeding. In addition, caged ducks are subjected to repeated close contact withthe force-feeder, who they cannot avoid, and to the forcible introduction of food into
the oesophagus, a novel and unpleasant sensation especially at the early stages when
the duck’s gag reflex still occurs. These experiences are likely to lead to failure of
ducks with ‘nervosisme’ to cope with their environment and with human contact andresult in poor welfare.

38

Other welfare considerations
The human-animal relationshipA widely held view in many communities is that farm animals can suffer, and thatanimal suffering is the most important consideration in our moral obligations towards
animals (Hemsworth 2007). Frequently raised concerns about farm animal welfare
include indoor housing, confinement and routine husbandry procedures (Hemsworth
2007, Broom and Fraser 2015); these have been highlighted in this review.
Stockmanship, in contrast, receives less attention even though stock people have amajor impact on the welfare of their livestock.
There is substantial evidence that negative interactions between humans and animals
increase the animals’ fear and stress (Hemsworth 2007). In the case of foie gras
production, the relationship between the force-feeder and the force-fed ducks hasreceived little attention. Perhaps this is because the force-feeder is often only involvedin the final stage rather than in the whole production process, and because their work
is normally restricted to force-feeding and cleaning activities. Concerns have beenraised that, with the obligatory introduction of group housing in 2016, the work of theforce-feeder will take longer and be more difficult. Not surprisingly, Litt (2010) foundthat force-feeding took longer when birds were group housed than when in the small
cages with their heads sticking out. Workers had to modify their technique andmovements, and access to birds was more difficult. Due to the difficulties in catching
and restraining birds, a containment system of movable front and back walls has beendevised, which reduces the birds’ ability to struggle, resist or escape. This may makeforce-feeding quicker and easier, but causes fear and has a negative impact on thestockperson-animal relationship. Fearful animals are more difficult to handle and little
or no habituation to force-feeding is likely to occur.
Domestic animals usually develop a relationship with the person looking after them,especially if the person provides food and other positive resources such as bedding,and activities such as talking, petting and grooming. The need for containment of the
ducks, to bring them towards the force-feeder and to immobilise them, strongly
suggests that the ducks find restraint, the force-feeding procedure, the food being
force-fed and the force-feeder, aversive. The responses seen, such as struggling andescape behaviours, are typical of farm animals subjected to routine procedures thatthey find painful, frightening and unpleasant (Vinuela-Fernandez et al 2011). If ducks
were being offered acceptable food and did not find the procedure painful orotherwise aversive and the force-feeder frightening, there would be no need forcontainment. Instead, they would move forward voluntarily towards the force-feeder
and stay still while fed because food is a necessary and desirable resource.
Control over the environment and motivation
The foie gras industry speaks of ‘respect for the animal’ in the sense of considerationof its welfare, yet there is a clear failure to meet the duck’s needs. The duck is forced
to ingest food against its will, and is unable to regulate intake in terms of quantity or
quality. An important concept in relation to understanding animal welfare is thecontrol which an individual has over its environment (Broom 1991). Welfare is poorer

39when the individual lacks control, is affected by the consequences of lack of control
i.e. it fails to cope, or feels pain or fear (Broom 2008). This is relevant to foie gras
production; the animal lacks control over an aspect of its life that is crucial to its
survival, the acquisition and ingestion of appropriate quantities of an appropriate diet.
Force-feeding prevents the duck from performing its normal, species-specific foraging
and feeding behaviours, so its motivations to search for and ingest food in order toachieve satiety and homeostasis cannot be fulfilled. Motivated behaviours have twophases: an ‘appetitive’ phase in which the animals search or prepare for theopportunity to perform a ‘consummatory’ phase (Mason and Burns 2011). In the caseof food, their expression is vital to the animal’s survival so both phases are driven bystrong motivations, and emotions appear to be important in their control. Being unable
to satisfy strong motivations leads to frustration (Mason and Burns 2011). The
appetitive (foraging and dabbling) and consummatory (eating) behaviours of force-fed
ducks are prevented and this is likely to lead to frustration and poor welfare.
The European Charter and the Welfare Quality® projectIn 2008 the European Federation of Foie Gras, consisting of all the representatives offoie gras producing countries in the European Union, was signatory to a European
Charter on the “breeding of waterfowl for foie gras” (seehttp://www.eurofoiegras.com/docs/EUROFOIEGRAS_CHARTE_UK.pdf).
(Theterm ‘élevage’ is not translated accurately; the Charter is not about breeding but about
rearing and fattening, or production).
The Charter is derived from the twelve criteria of the Welfare Quality® project (seebelow). It is worth noting that the term ‘assisted feeding’ is used in the English and‘gavage’ in the French version of the Charter. The Federation claims that, “ifperformed by professionals under regulated conditions, gavage does not cause any
suffering to the animals” (see http://www.eurofoiegras.com/en/page/euro-foiegras_p134/). A support programme called ’Palmi G Confiance’ was created in 2014 tohelp foie gras producers meet the standards of the European Charter with regard toanimal welfare and good practice.
The four welfare principles and 12 criteria proposed by the Welfare Quality® project(Blokhuis et al 2010) are a development of the Five Freedoms concept (Broom andFraser 2015). They present general guidelines on the needs of animals and how they
may be met. A need is a requirement, which is part of the basic biology of an animal,
to obtain a particular resource or respond to a particular environmental or bodily
stimulus (Broom 1996, Broom and Fraser 2015).
While the Welfare Quality® assessment system emphasises the use of animal-based
measures, it also includes important resource-based and management-based ones.
Between 30 and 50 measures are collected and categorised into 12 criteria which arefurther integrated into 4 welfare principles: good feeding, good housing, good healthand appropriate behavior.
The Welfare Quality® assessment system is criticised for taking a long time toperform and being overly complicated (Leterrier et al 2015). Researchers are working
with the whole poultry industry to develop a simple method that can be used on alarge scale and is largely based on animal measures. Some research is focussed on
identifying measures easily taken in the abattoir that are highly correlated withmeasures on-farm that are more difficult to collect (Litt et al 2015a). While thisapproach may be premature for ducks kept for foie gras production, due to the40

imminent changes in housing and the lack of good physiological and behavioural datafrom group-housed birds, we have made a preliminary attempt at assessing thewelfare of ducks in foie gras production using the Welfare Quality® assessment
system (Table 1, next page)). Based on the information available to us, and contrary
to the aspirations of the European Charter, only three of the 12 criteria and none of thewelfare principles are met in current systems of foie gras production.
Other stages of foie gras production
While the primary aim of this review has been to highlight the welfare problems in
the last stage of foie gras production, when ducks are force-fed, welfare problems
have also been identified in the first two stages, starter and growth. These include theearly, frequent and rapid development of footpad dermatitis, hock burns and breast
blisters, fear of humans and high sensitivity to the environment, and lack of access toopen water for bathing or at least full immersion of the head. It seems that undercommercial conditions water is normally only provided by nipple drinkers, despite
ducks being aquatic animals who spend most of their lives close to or on water(RSPCA 2015, Broom and Fraser 2015). The Council of Europe (1999) requirements
for ducks state that they should be able to dip their heads in water and spread waterover their feathers; this is possible with baths, troughs and showers but not withnipple or bell drinkers. If properly managed, the provision of open water as baths,
troughs or showers should not lead to disease. On the contrary, a good open water
system can improve eye, nostril and feather condition, and reduce disease (Jones et al
2009; O’Driscoll and Broom 2011, Liste et al 2012).

41

Table 1. Principles and criteria that underpin the Welfare Quality® assessment system
Welfareprinciples
Good feeding

Good housing

Good healthAppropriate
behaviour

Criterion
Animals should not suffer fromprolonged hunger, i.e. they shouldhave a sufficient & appropriate diet.

Is
met?
No

Animals should not suffer fromprolonged thirst, i.e. they shouldhave a sufficient & accessible watersupply.
Animals should have comfort aroundresting.

Yes

Animals should have thermal
comfort, i.e. they should neither be
too hot nor too cold.
Animals should have enough space
to be able to move around freely.

No

Animals should be free of physicalinjuries.
Animals should be free of disease,i.e. farmers should maintain highstandards of hygiene & care

No

Animals should not suffer pain
inducedbyinappropriate
management, handling, slaughter, or
surgical procedures (e.g. castration,
dehorning).
Animals should be able to express
normal,non-harmful,socialbehaviours, e.g. grooming.

No

Animals should be able to express
other normal behaviours, i.e. it
should be possible to express
species-specific natural behaviours
such as foraging.
Animals should be handled well inall situations, i.e. handlers should
promotegood
human-animal
relationships.

No

Negative emotions such as fear,
distress, frustration or apathy shouldbeavoidedwhereaspositive
emotions such as security orcontentment should be promoted

No

No

Yes

No

Yes

No

it

Example of how criterion is or is
not metDuck is fed a diet that is neither
appropriate nor sufficient; it cannot
regulate its intake to achieve satiety& homeostasis
There may be problems withmaintaining cleanliness, ensuringease of access to water troughs &trough design
There is no resting area & no
bedding, the floor consists of wire orplastic mesh
There is thermal stress due to large
amounts of high energy food leading
to prolonged panting
More behavioural research isnecessary to confirm optimal cage
size & design & stocking density
Injuries due to containment, capture,handling & force-feeding occur
Footpad & hock dermatitis, lesions tobreastbone are frequent & often
severe; liver steatosis is caused
deliberately
Containment, capture, handling &force-feeding may be sources of pain;high prevalence of wing lesions
caused by handling & transport toabattoirFurther research needed on social
behaviour in group housing, optimalgroup size & social behaviours, signsof good welfare
There is no substratum for foraging;further research is necessary on theuse of water troughs, dry & wet
preening & grooming behaviours
Catching & handling for forcefeeding does not promote good
human-animal relationships; poor
handling during transport prior toslaughter causes wing lesions
Fear, distress, frustration, pain &other negative emotions are very
likely when ducks are subjected tothe stages of foie gras production,
especially at force-feeding. Problemof nervousness & hyper-reactivity inhybrid mulard ducks

42

Conclusions
From our review of the available scientific literature, we have reached the following
animal welfare-related and general conclusions:
Animal welfare-related
1. In 2006 the national average mortality of force-fed birds was 2.4% and in2013 it was 2.2%. The Institut Technique de l'Aviculture reports mortality of 2
to 5%. These data compare unfavourably with mortality rates of muscovy
ducks in fattening units in the UK, where in the two weeks before slaughter
the mortality rate was 0.2%.
2. Birds in foie gras production are the only farmed animals that are not allowed
to use their basic biological mechanisms to regulate their own food intake.
3. Ducks are motivated to perform normal foraging activities, such as searchingfor food, pecking, nibbling, dabbling, up-ending and swallowing. Their need
to forage is not met during force-feeding.
4. Since force-feeding prevents the duck from performing its species-specificforaging and feeding behaviours, its motivations to search for and ingest foodcannot be fulfilled and, as in many other species, this is likely to lead tofrustration.
5. Ducks are fed such large amounts of food that they are unable to maintainsatiety and homeostasis. They are denied the opportunity to show normal
feeding behaviour in accordance with their appetite.
6. With force-feeding the duck lacks control over an aspect of its life that is
crucial to its survival, the ingestion of appropriate quantities of an appropriate
diet. Loss of control leads to very poor welfare.
7. Force-feeding causes the birds to become obese, leading to foot and leg
disorders that reduce their ability to move and are likely to be painful.
8. Force-feeding may cause injury and pain to the bill, face, eyes, nostrils, neckand upper digestive tract. However, descriptive studies of these conditions arelacking.
9. Bone fractures and other wing lesions are common and are most likely tooccur at the stages of collection, transport to the abattoir and shackling.
10. Ducks are force-fed large amounts of an unbalanced diet that does not meettheir nutritional needs and leads to significant liver, bone and other pathology.

43

11. Force-feeding causes a degree of liver pathology, especially steatosis (fatty
liver), that is desirable and of value to producers of foie gras but greatly
increases the duck’s risk of premature death.
12. There is clear evidence of liver pathology: a reduction in the liver’s ability todetoxify, (slower BSP clearance, longer BSP half-life) and liver cell damage(raised liver enzymes) at the end of the force-feeding period. The reversibilityof steatosis does not mean that the changes in the liver are not pathological.
13. Force-feeding a nutrient-deficient diet in large amounts leads to grosshepatomegaly (liver enlargement), which can cause pain and difficulties inbalancing and movement.
14. The enlarged liver may compress respiratory airsacs and other abdominalorgans, and where liver function is severely compromised hepatic
encephalopathy (effects of toxins on the brain) may ensue.
15. Due to the large amount of high-energy food, ducks are placed underconsiderable thermal stress. They spend a large proportion of their time
panting in order to thermoregulate and maintain physiological homeostasis.
16. Levels of blood corticosterone are a poor indicator of welfare if measured inassociation with feeding in mulard ducks. They must be considered inconjunction with other welfare indicators such as health, pathology, otherphysiological measures, behaviour and other indicators of mental state.
17. Individual cages greatly restrict the bird’s movements and do not allow it toshow more than a minimal behavioural repertoire, with consequent very poor
welfare.
18. Ducks are gregarious and require cages big enough so that they are able tofully stretch their wings, preen and groom, walk and show normal social
interactions and other behaviours. Group cages are small, usually offering asurface area per bird of only 1200-1300 cm2.
19. Group cages are barren, containing only conspecifics and water troughs. It is
not clear whether the water troughs currently used allow full immersion of the
duck’s head and the normal bathing that is essential for preening.
20. Contrary to Council of Europe recommendations and the European Federationof Foie Gras Charter guidelines, group cages do not contain litter. Thisdeprives the ducks of substratum for foraging and exploratory behaviours.
21. Contrary to Council of Europe recommendations and the European Federationof Foie Gras Charter guidelines, group cages do not have an area where ducks
can rest together, and there is no bedding material to ensure their comfort andcleanliness.
22. The group cage has a steel or plastic mesh floor that may worsen contact
dermatitis (foot, toe, hock and breast lesions).

4423. Due to the difficulties in catching and restraining birds for force-feeding, acontainment system has been devised which reduces the birds’ ability to
struggle, resist or escape. This makes force-feeding quicker and easier, butcauses fear and has a negative impact on the stockperson-animal relationship.
24. Group-housed birds may be more susceptible to injury from poor forcefeeding technique, handling, getting caught in the cage’s containment
mechanism, or restrained in a bad position for a long time.
25. The condition of ducks deteriorates as they pass through the successive stagesof foie gras production. Painful skin lesions such as contact dermatitis are
frequent and develop early in the production process. They are often severe by
the force-feeding stage, and other body injuries also occur.
26. Ducks in the first two stages of foie gras production, starter and growth(rearer), may not have access to open water for bathing, or at least for fullimmersion of the head, despite having a need for open water to maintainplumage and body condition and to thermoregulate.
27. Compared with controls, force-fed ducks show a variety of behaviouralchanges which indicate poor welfare such as lack of mobility, increased timelying down, reduced grooming and preening and social interactions, andprolonged panting.
28. The oropharynx in birds is adapted to perform the gag reflex to prevent
material from entering the throat except as part of normal swallowing, andprotects against choking and aspiration. Initially, force-feeding stimulates thisreflex but after a certain time it stops. The adaptation time required for the gag
reflex to be extinguished, and how the duck is affected by this, are not known.
29. Ducks are fed by having a tube forcibly inserted into their oesophagus twice
daily for up to 15 days. They are reluctant to enter a pen where they are forcefed, an indication that they find force-feeding aversive. There is no convincing
evidence that ducks show a lesser avoidance response to the force-feeder thanto another (unfamiliar) person.
30. Other duck welfare problems include fear of humans and a high degree of
nervousness and reactivity to the environment. Reactive, nervous and fearfulducks are less well able to cope, with consequent poor welfare.
31. With current methods of foie gras production, only three out of 12 criteria andnone of the welfare principles described in the Welfare Quality® project are
met.
General
1. In the last 10 years in France, national production of foie gras has increased by
11%, from 17,217 tonnes in 2003 to 19,067 tonnes in 2013 with 98% comingfrom ducks. Profit margins have decreased as costs have increased.

45

2. Migratory birds have mechanisms for storing food before migration. The
greylag goose Anser anser, traditionally the main species used for foie gras
production, is migratory. The muscovy and the mulard duck are non-migratory
and most populations of wild mallard migrate little. Pre-migration foodstorage may lead to liver size increase but probably not more than a doublingof size.
3. By the end of the force-feeding period, the duck’s liver is 7 to 10 times thesize of a normal liver with an average weight of 550 to 700 g and a fat content
of 56%. This increase in liver weight is accompanied by a live-weight gain in
the range of 50 to 85%.
4. Fatty liver results from an increased capacity of hepatic lipogenesis, aninsufficient hepatic capacity to export newly synthesised triglycerides, and alimited capacity of peripheral tissues to take up circulating lipids, thus
favouring their return towards the liver.
5. Spontaneous over-eating in geese can be stimulated by manipulating day
length and feeding regimes, usually restriction followed by ad-libitum feeding,and may eventually become a method of foie gras production that does not
require force-feeding.
6. Due to the difficulties in catching and restraining group-housed birds forforce-feeding, a containment system has been devised which reduces thebirds’ ability to struggle, resist or escape. It consists of a movable back wall
which pushes the birds towards the front, and a front vertical wall which
descends over them and prevents them from escaping or moving much(‘peigne de contention’).
7. Compared with individual housing, group housing leads to a decrease in liver
weight, an increase in the weight of the ‘magret’, an increase in the time taken
to perform the force-feeding and an increase in the amount of water used incleaning. At slaughter, there are more liver defects and fewer haematomas but
more scratches on the duck’s carcass.
8. The consumption of foie gras may have negative effects on humans. Duck orgoose-derived foie gras contains amyloid protein which could hasten thedevelopment of amyloidosis in a susceptible population.

46

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