caging of ducks for foie gras production in France was replaced by group (collective) 51!
housing, with at least 3 birds per group (Anon 2015). This review, which focuses on 52!
foie gras production in France, highlights the welfare problems that may arise in the 53!
final (third) stage of foie gras production, when force-feeding occurs. Where pertinent, 54!
welfare problems that may arise in the first two stages are also described. 55!
We focus on research in ducks rather than geese because ducks are used in over 97 % 56!
of foie gras production in France (18,600 tons in 2013, Litt & Pé 2015). Most of the 57!
foie gras literature is in French. Foie gras producing countries in the European Union 58!
are France, Belgium, Bulgaria, Hungary and Spain (Litt & Pé 2015), producing 59!
approximately 90% of the world’s foie gras. Force-feeding of ducks and geese for foie 60!
gras is banned in a large number of European and other countries, but many countries 61!
where production is banned continue to import it. 62!
The terms force-feeding and gavage are used interchangeably here. Other terms, such 63!
as assisted feeding, cramming and over-feeding, are sometimes used in the literature. 64!
The main food used, maize, is usually called corn in North America. In some 65!
instances approximate translations are used, because the equivalent English word does 66!
not seem to exist (eg ‘nervosisme’). The term ‘élevage’ means rearing or breeding but 67!
is also used to describe stages of production (eg starter, grower). 68!
Background information 70!
The male mulard duck, the mulard being a hybrid between a muscovy drake (Cairina 72!
moschata) and a female domestic duck (Anas platyrhynchos) which is a mallard, is 73!
used most frequently for force-feeding because it has a good potential for production 74!
and is relatively easy to manage when housed individually (Guémené & Guy 2004). 75!
The breed of domestic duck/mallard most often used is the Pekin, so this name will be 76!
used here unless specified otherwise. In France only male mulards are usually reared 77!
for foie gras production (Baéza 2006), while females are killed once they have been 78!
identified following hatching. This is because their fatty livers are of poor quality and 79!
therefore unsuitable as a product with the appellation “100% foie gras” (Marie-80!
Etancelin et al 2015). 81!
The process of foie gras production in France is described in SCAHAW (1998), 82!
Guémené and Guy (2004), Rodenburg et al (2005) and Guémené et al (2007). Briefly, 83!
it can be divided into three stages: 84!
1. Starting: Birds are fed ad libitum from the time of hatching until 6 to 9 weeks. They 85!
are initially kept indoors, usually on straw, and eventually allowed outdoors during 86!
the day. 87!
2a. Growing: Birds are feed-restricted for a period of 3 to 5 weeks. This restriction 88!
may be in time (hourly feed restriction, when birds are fed ad-libitum but for only a 89!
short period, once daily) or amount (quantitative feed restriction, when birds are fed a 90!
reduced amount of food daily). Birds normally have outdoor access during the day. 91!
2b. Pre-force-feeding: Birds are fed as much as possible for 3 to 10 days. The aim is 92!
to dilate the oesophagus and stimulate the digestive secretions necessary for the 93!
assimilation of a large amount of food, and start the process of liver steatosis. The 94!
liver can weigh up to 180 g by the end of this stage, compared with 80 g with normal 95!
feeding. Ducks usually have outdoor access during the day. 96!
3. Force-feeding: From 12 weeks of age and usually for 12 to 15 days, ducks are 97!
force-fed increasing amounts of energy-rich food with a high carbohydrate, low 98!
protein content and an abnormal amino acid and mineral balance (AVMA 2014). 99!
They are force-fed twice daily with a feeding tube powered by a pneumatic or 100!
hydraulic pump; at the beginning each receives 180 to 200 g of maize per meal, 101!
increasing to 450 g (1000 g after water is added to make mash) per meal towards the 102!
end of the force-feeding stage. Up to 400 individually caged ducks per hour can be 103!
force-fed by one person using a pneumatic pump (Guémené & Guy 2004), and even 104!
more if a hydraulic dispenser is used. They are kept indoors in cages and in a 105!
controlled environment. 106!
Literature Search 108!
In order to find peer-reviewed literature on the force-feeding of ducks, we conducted 110!
a search of the following databases: Medline (PubMed, US National Library of 111!
Medicine), Google Scholar (Google), Scopus (Elsevier), VetMed Resource (CABI, 112!
Centre for Agriculture and Bioscience International) and Web of Science (Thomson 113!
Reuters). Each search had the same terms, which were used as subject headings and as 114!
keywords. How they were combined varied, depending on the database stipulations. 115!
While we focussed on peer-reviewed published research, we also made use of ‘grey’ 116!
literature such as technical reports, and other material that may not have been 117!
subjected to editorial control or peer review. The report by SCAHAW (1998) 118!
provided background information and served as a useful guide on potential welfare 119!
topics to consider. Only publications in English or French were included. 120!
The proceedings from the biennial conferences “ Journées de la Recherche sur les 121!
Palmipèdes à Foie Gras” were a rich source of information on research covering a 122!
wide range of aspects of foie gras production, including welfare. Of the 78 references 123!
included in this review, 25 are proceedings from these conferences. This material 124!
helped us identify the main researchers in the field and the current research topics. 125!
These conferences are supported by a number of organisations, such as the research 126!
institutes ITAVI (Institut Technique de l'Aviculture et de l'Elevage des Petits 127!
Animaux) and INRA (Institut National de la Recherche Agronomique). 128!
The welfare issues we have identified are organised under six main headings: 129!
mortality, physical health, general behaviour, force-feeding, housing and other. 130!
Limited mortality figures are available for ducks during the two-week force-feeding 134!
period (Servière et al 2011) and it is difficult to find a reasonable baseline for 135!
comparison, such as the mortality rate of non force-fed mulard ducks. SCAHAW 136!
(1998) concluded that mortality during the force-feeding period was typically 2 to 4%. 137!
In 2006 the French national average mortality of force-fed birds was 2.4% (Laborde et 138!
al 2010) and in 2013 it was 2.2% (Litt & Pé 2015). 139!
In an experimental study exploring the effects of group size and stocking density on a 140!
number of production measures during force-feeding, average mortality was 5.6% 141!
(range 1.4-13.9) (Mirabito et al 2002a). The highest mortality was seen in the largest 142!
group (9 birds) with the highest stocking density (1000 cm2 per bird). These data 143!
compare unfavourably with mortality rates of muscovy ducks in fattening units for 144!
meat production, where in the two weeks before slaughter the mortality rate was 0.2% 145!
(SCAHAW 1998). 146!
Physical health 148!
The health of birds can be assessed using a wide range of variables including gross 150!
body anatomy, posture, walking ability (gait), face, body and plumage condition, 151!
presence of bone fractures, presence and severity of skin lesions as well as mortality 152!
(Jones & Dawkins 2010a; Liste et al 2012; Makagon et al 2015; Saraiva et al 2016). 153!
There are few such studies in force-fed ducks (but see Litt et al 2015 a, c). 154!
Gait means walking ability, and is often recorded as an on-farm measure of welfare in 155!
poultry raised for meat (Bradshaw et al 2002, Makagon et al 2015). Impaired gait can 156!
cause poor welfare because of its association with pain (Saraiva et al 2016), and is 157!
economically important as ducks with moderate to severe walking problems are often 158!
culled from the flock (Makagon et al 2015). A number of gait score systems have 159!
been developed for use in ducks (Jones and Dawkins 2010a; O’Driscoll & Broom 160!
2011; Liste et al 2012; Makagon et al 2015; Saraiva et al 2016). They need to be 161!
standardised so that meaningful comparisons between studies can be made. 162!
When birds are kept in restrictive environments where they cannot move freely, 163!
recognising mobility problems becomes difficult. Anecdotal observations by 164!
SCAHAW (1998) suggest that abnormalities in posture and gait in fattened ducks 165!
occur to the extent that some die from becoming immobile and unable to access water. 166!
The legs of force-fed birds are pushed outwards, so that they cannot be held vertically 167!
when the bird is standing or walking. SCAHAW concluded that this is caused by the 168!
hypertrophy of the liver, which pushes the legs laterally and causes difficulty in 169!
standing and impairment of their natural gait. 170!
Recently Litt et al described the development (2015a) and application (2015c) of an 171!
evaluation grid (‘grille d’évaluation’) to assess the physical condition of mulard ducks. 172!
A subjective scoring system with three or four degrees of severity for each measure 173!
was used. The grid was applied to 63 groups of ducks on 44 different commercial 174!
farms at the end of each of the three main stages of production. Birds in the force-fed 175!
group were evaluated after slaughter in an abattoir. Four main physical abnormalities 176!
were noted at all stages: dermatitis of the footpad, toe (digit) and hock (hock burn), 177!
and damage to the breast area. Breast abnormalities included loss of feathering and 178!
lesions (blisters, ulceration and the formation of crusts). Ventral feathering loss was 179!
more commonly noted during the growth stage while breast lesions were noted after 180!
slaughter. Footpad and toe dermatitis lesions appeared very early and very frequently 181!
in the production process. Wing lesions were noted at the end of force-feeding; 88% 182!
of lesions probably occurred at the stages of collection, transport to the abattoir and 183!
shackling. Other body injuries, such as scratches to the dorsal part of the body, 184!
pseudo-crop injury (lacking a defined crop, the mulard has an oesophageal out-185!
pouching called the pseudo-crop) and joint abnormalities, were also noted after 186!
slaughter. Litt et al (2015c) concluded that the most useful measures were the 187!
presence and severity of dermatitis of the footpad and digits, the condition of the 188!
breast, back injuries (eg scratches or haematomas) and injuries to the pseudo-crop. 189!
Overall, the prevalence of lesions varied greatly between farms and groups of birds, 190!
and associations with fixed factors such as starter density and season were not 191!
sufficient to explain this variability. 192!
Comparisons between Litt et al’s (2015c) evaluation grid and other studies in ducks 193!
reared for meat should be made with caution. Force-fed ducks are housed and 194!
managed very differently, and are fattened for much longer. What is clear is that the 195!
welfare of force-fed ducks, as assessed by general physical condition, deteriorated 196!
significantly as they progressed through the three production stages. 197!
In a survey of Pekin ducks commercially reared for meat in the UK, the physical and 198!
plumage condition of the ducks was recorded at two ages, 23 and 41 days (Jones & 199!
Dawkins 2010a). The birds’ condition deteriorated between 23 and 41 days, but this 200!
was not marked. At slaughter, the incidence of moderate and severe footpad 201!
dermatitis lesions was 10% and 3%, 32% of ducks had calloused toes and 11% had 202!
pink hocks. In other commercial trials evaluating open water sources for farmed 203!
ducks over 43 days, contact dermatitis lesions were mild and general condition good 204!
(O’Driscoll & Broom 2011; Liste et al 2012). In contrast, Litt et al (2015b) found that 205!
by 14 weeks of age, the end of force-feeding, all the duck foot samples had moderate 206!
to severe macroscopic signs of epidermal ulceration. Pododermatitis was common, 207!
and developed early in the birds’ lifetime. Biija et al (2013) studied ducks during the 208!
period prior to force-feeding, when they were allowed outdoor access either onto a 209!
meadow with scattered trees or onto woodland. At 9 and 11 weeks of age both groups 210!
(especially the one with woodland access) had developed moderate to severe 211!
An increase in enteric flora load and in faecal streptococci, causing gastro-intestinal 213!
upset and diarrhoea, has been noted at the beginning of force-feeding. Enteric flora 214!
overgrowth and infections can exacerbate any existing contact dermatitis and cause 215!
death in force-fed birds (Laborde et al 2010). 216!
Contact dermatitis is an umbrella term that includes footpad and toe dermatitis (also 217!
known as pododermatitis or foot burn), hock burns and breast blisters and burns in 218!
poultry (Shepherd & Fairchild 2010; Hepworth et al 2011). It is a condition which 219!
causes pain and disability (Haslam et al 2007; Saraiva et al 2016), leading to poor 220!
welfare and significant economic loss. Animal welfare audits often include contact 221!
dermatitis as an indicator of housing conditions and bird welfare (Haslam et al 2007; 222!
Hepworth et al 2011; Saraiva et al 2016); this may be useful for foie gras ducks too. 223!
Reports of post-mortem examinations of ducks that die during or at the end of force-224!
feeding are sparse in the published scientific literature. There is little information on 225!
injuries, disease incidence and nature, causes of death, the incidence of secondary 226!
oesophageal infections (such as Candidiasis, a yeast infection caused by Candida 227!
albicans) or on other complications that may arise. SCAHAW (1998) reported that 228!
secondary infections with C.albicans was present in up to 6% of birds. 229!
General Behaviour 231!
Mulard ducks are most often used for foie gras production, despite being recognised 233!
as particularly fearful, nervous and hyper-reactive – the term ‘nervosisme’ is used in 234!
French. These behaviours become evident at 5 to 7 weeks of age (Guémené et al 235!
2002). Birds show panic and flight responses to the approach of humans and are 236!
generally described as being ‘sensitive to the environment’ (Guémené et al 2002; 237!
Guémené et al 2006b; Laborde & Voisin 2013). It seems that the move from 238!
individual to group housing has brought the problem of ‘nervosisme’ in ducks to the 239!
fore. Certain behavioural characteristics of mulards are recognised: while ducks are 240!
gregarious and sociable towards conspecifics (Guémené et al 2006b), making group 241!
housing enriching, they are fearful of humans, nervous, and highly reactive to their 242!
environment (Laborde & Voisin 2013). Therefore, they are less well able to cope with 243!
environmental changes and with the presence of humans. They struggle and try to 244!
escape when approached for force-feeding thereby necessitating the use of crowd-245!
French scientists have established a research project called “CaNervosisme” to 247!
address these undesirable characteristics. The project includes a large number of 248!
different experiments looking at factors such as the birds’ phenotype, genotype, 249!
genetic manipulations, provenance, rearing conditions, group size, behavioural and 250!
physiological responses and exposure to humans (Guémené et al 2002; Faure et al 251!
2003; Guémené et al 2004; Guémené et al 2006b; Arnaud et al 2008; Laborde & 252!
Voisin 2013). For example, Arnaud et al (2008) found that mulards showed greater 253!
panic responses and fear of humans, and appeared to be more sensitive to social stress 254!
(isolation from other ducks) than the two parent types, evidence of heterosis. A 255!
heterosis effect was also found for basal adrenal activity, with mulards having higher 256!
basal levels of corticosterone than parental lines. 257!
There are many aspects of husbandry and practice prior to force-feeding that may 258!
affect the birds’ behaviours during force-feeding, but effects are not clear-cut. 259!
Nevertheless, it seems that ‘nervosisme’ has two main components: fear of humans 260!
and fear of the environment. Because foie gras production involves close human 261!
contact and sudden environmental changes, it has severe negative effects on the birds’ 262!
A major objection to the practice of foie gras production is that, unlike other farmed 267!
animals, the birds cannot choose what, when and how much they will eat. They 268!
cannot show a food preference or feed spontaneously, and are fed considerably more 269!
than they would eat voluntarily. They receive this food without having the 270!
opportunity to forage in a species-specific manner. 271!
Force-feeding, where the duck is restrained and a rigid tube is inserted into the 272!
oesophagus, has the potential to cause injury and pain so the condition of the upper 273!
digestive tract is of particular interest. A number of studies have looked for 274!
histological evidence of pain at different stages of force-feeding. Servière et al (2002) 275!
described signs of sub-acute moderate and multifocal oesophagitis, which may be a 276!
result of effects of abrasion and distension of the upper digestive tract caused by food 277!
boluses. In other experiments, force-fed ducks were compared with 278!
pharmacologically-treated control ducks, in which neurogenic inflammation of the 279!
upper digestive tract was provoked under anaesthesia by an irritating substance 280!
containing mustard oil (Servière et al 2002) or hydrochloric acid (HCl) (Servière et al 281!
2011). For example, in Servière et al (2011) varying concentrations of HCl were 282!
applied to different parts of the upper digestive tract and the resulting neurogenic 283!
inflammatory response compared with that due to the force-feeding regime. 284!
Neurogenic inflammation describes the local release of inflammatory mediators from 285!
afferent neurons upon activation of sensory nerve fibres (Rosa & Fantozzi 2013). 286!
These neuropeptides cause an inflammatory response characterized by plasma 287!
extravasation, local vasodilatation, leukocyte and platelet adhesion, and mast cell 288!
degranulation. By measuring degrees of the extravasation response in both groups, the 289!
authors concluded that the mechanical insult to upper digestive tract walls due to the 290!
force-feeding regime is moderate compared with chemical nociceptive stimulation 291!
with HCl. 292!
One may question whether the above experiments are a good way of evaluating pain 293!
caused by force-feeding. The irritating substances may not produce standardized 294!
inflammatory responses (and consequent pain) with which force-feeding effects can 295!
be compared. Mechanical stimulation, such as excessive distension, may also induce 296!
visceral nociception. Detailed post-mortem examination of the upper digestive tract 297!
and other body areas may be more informative, as well as behavioural observations. 298!
Recording facial and body lesions is particularly relevant, as it seems that the 299!
likelihood of injury may increase in group-housed birds because of the need to catch, 300!
position and restrain them (Guémené et al 2002; Guémené et al 2006b). !301!
Effects on the liver 303!
The potential to develop hepatic steatosis depends on the species of waterfowl and 305!
also varies with the genotype (Baéza et al 2013). Some migratory waterfowl, such as 306!
greylag geese Anser anser, eat more than their normal amount of food in the days 307!
before migration. The muscovy and the mulard duck, however, are non-migratory and 308!
do not develop a hypertrophied liver when reared normally. Force-feeding results in 309!
an increase in liver size and fat content. By the end of force-feeding, the duck’s liver 310!
is 7 to 10 times the size of a normal one with an average weight of 550 to 700 g and a 311!
fat content of 55.8% (Babilé et al 1996; Gabarrou et al 1996). This increase in liver 312!
weight is accompanied by a substantial overall live-weight gain in the range of 50 to 313!
85%. In comparison, the average weight of a non force-fed drake’s liver is 76 g with a 314!
fat content of 6.6% (Babilé et al 1996). 315!
Steatosis and other changes that occur as a result of general management for foie gras 316!
production, in particular force-feeding, are pathological and can limit the ducks’ 317!
survival potential. The enlarged liver may cause discomfort, compress airsacs 318!
(reducing respiratory capacity) and abdominal organs. When liver function is severely 319!
compromised, hepatic encephalopathy (central nervous dysfunction due to effects of 320!
toxins such as ammonia on the brain) may develop (SCAHAW 1998). 321!
A detailed illustration of the steatosis process is presented in Baéza et al (2013). 322!
Steatosis results from an increased capacity of hepatic lipogenesis and insufficient 323!
capacity to export newly synthesised triglycerides, resulting in their accumulation in 324!
hepatocytes. Peripheral tissues cannot take up sufficient circulating lipids, thus 325!
favouring their return towards the liver. Hepatocytes hypertrophy due to accumulation 326!
of fat and other components (water, minerals, proteins, phospholipids). Lipid 327!
synthesis in the liver is maximised when the food is high in starch and low in protein, 328!
such as maize. Maize also has high levels of thiamine and biotin, which are necessary 329!
for the conversion of sugars to lipids. To reduce the ducks’ capacity to make Very 330!
Low Density Lipoprotein, which carries lipids away from the hepatocytes to 331!
peripheral tissue, the diet is restricted in levels of certain nutrients necessary for their 332!
synthesis such as amino acids methionine and choline (Gabarrou et al 1996). Force-333!
feeding a high-energy, high carbohydrate diet turns a normal liver into a steatotic one 334!
in under two weeks (Gabarrou et al 1996). 335!
In an experiment by Babilé et al (1996), mulard ducks were force-fed for 10, 13 and 336!
16 days, and at the end of each period were released back into the group. For the first 337!
few days they did not eat but drank copiously, and lost a lot of weight in the first 338!
week. The longer the force-feeding period, the longer it took for ducks to start eating 339!
spontaneously again (8 to 15 days). The liver returned to its initial weight after 15 340!
days following the end of force-feeding for groups force-fed for 10 and 13 days, and 341!
took 30 days for those force-fed for 16 days. These results give an insight into the 342!
degree of insult from which the liver had to recover. Prolonging the force-feeding 343!
from 13 to 16 days has a disproportional effect on time to liver weight recovery (an 344!
increase from 15 to 30 days), suggesting that 16 days of force-feeding brings the duck 345!
close to severe liver dysfunction and failure. 346!
Bénard et al (1998, 2006) examined the effects of force-feeding on liver function, 347!
morphology and pathology. Group-housed ducks were force-fed for 2 weeks and then 348!
received normal ad-libitum feeding for 4 weeks. This cycle was performed three times, 349!
with force-fed birds compared with a control group fed ad-libitum throughout. Blood 350!
samples were taken at the end of every force-feeding or free-feeding cycle from the 351!
test birds and at the same time from controls. A bromosulphophthalein (BSP) 352!
clearance test, a measure of the liver’s ability to detoxify, was also performed. Birds 353!
were killed after 2, 6, 8, 12, 14 and 18 weeks and their livers examined. 354!
While the weight of the non force-fed birds did not change significantly, the test 355!
ducks put on weight (1.5 to 2 kg), but lost it during the 4-week non force-feeding 356!
period (1.4 to 2.3 kg). Gross hepatomegaly was noted in force-fed birds and 357!
concentrations of liver enzymes lipase, alanine aminotransferase and aspartate 358!
aminotransferase rose significantly at the end of each force-feeding period. After 4 359!
weeks of normal feeding they returned to levels similar to those of the control group. 360!
After 2 weeks of force-feeding, hepatocytes in control birds had an average diameter 361!
of 7-10 µm whereas signs of steatosis were obvious in force-fed birds: hepatocyte 362!
diameter was 35-40 µm and the cell was full of fat vacuoles. After 3 cycles of force-363!
feeding the liver structure was similar, but 4 weeks later most of the liver cells had an 364!
average diameter similar to that of controls, and were no longer full of fat. BSP 365!
clearance, as measured graphically by the area under the curve, was reduced in force-366!
fed birds at 2 and 8 weeks compared with controls, while it returned to normal after 367!
periods of free-feeding as well as after the third force-feeding cycle. The elimination 368!
half-life (T½) of BSP was greatly prolonged at the end of each force-feeding period 369!
but returned to normal (values same as controls) after 4 weeks of free-feeding. 370!
The authors concluded that since animals were able to withstand three consecutive 371!
cycles of force-feeding with four-week intervals of normal feeding, and that no 372!
pathology was found after these rest periods, force-feeding does not induce diet-373!
related pathological changes since the steatosis was reversible. Consequently, animal 374!
welfare is not adversely affected. However, we argue that survival after a problem 375!
does not mean that the problem was of no significance. While steatosis was reversible 376!
in the studies described above, its reversibility does not mean that the liver changes 377!
were not pathological. The reduction in the liver’s ability to detoxify at the end of the 378!
force-feeding period, as indicated by a slower BSP clearance, longer BSP half-life and 379!
raised liver enzymes, is clear evidence of clinical pathology. These and various other 380!
data show that the steatosis obtained by force-feeding induces an impairment of 381!
hepatic function (SCAHAW 1998). In Babilé et al (1996), liver weight after 16 days 382!
of force-feeding took 30 days to reduce to normal, and in other studies the mortality 383!
of ducks increased when the force-feeding period was prolonged beyond 15 days 384!
(SCAHAW 1998). 385!
There are other points in the articles by Bénard et al (1998, 2006) that deserve 386!
attention. Force-feeding was performed on ducks housed in groups on the floor, by 387!
one person seated on a stool within their pen. This force-feeding is not typical of 388!
current practice (Litt 2010), taking much longer, about 30 seconds. The birds were 389!
closely examined twice daily throughout the study; force-fed birds were kept on wire 390!
mesh floors and developed signs of tibio-tarsal arthritis as well as skin calluses on 391!
their feet. These lesions disappeared when they were returned to straw litter for free-392!
feeding. After an initial 3-day period of agitation they showed increasingly longer 393!
periods of rest between each force-feeding, as well as an increase in wing flapping; 394!
the authors do not explain these behavioural changes. Agitation and wing flapping 395!
may be due to pain or fear, increasingly longer periods of rest due to pain, lethargy or 396!
abdominal discomfort. Hypertrophied livers can cause discomfort in a number of 397!
other species and this may also occur in ducks (SCAHAW 1998). There is no mention 398!
of access to water troughs for head immersion and wet preening, and despite close 399!
examination twice daily, the state of the ducks’ face, eyes and nostrils are not 400!
described. The results of this study do not support the authors’ conclusion that force-401!
feeding did not cause suffering. 402!
We suggest that additional physiological measures could be used in the assessment of 403!
liver function in force-fed ducks such as bile acids, ammonia, urea nitrogen, gamma 404!
glutamyltransferase, uric acid and coagulation factors in the blood and ketones in the 405!
blood or urine (Harr 2005). These measures are commonly used in other species. In 406!
addition, because maize is not a balanced diet for ducks other abnormalities may be 407!
present, such as hormone imbalances or altered calcium to phosphate ratios leading to 408!
bone pathology (SCAHAW 1998), so these should be measured too. 409!
Effects on behaviour 411!
Compared with physical and physiological effects, there is an even greater lack of 413!
published data on the behavioural responses to force-feeding both during the 414!
procedure itself and at other times, eg immediately beforehand when the ducks 415!
anticipate a potentially unpleasant experience, and afterwards when they have to 416!
digest a large amount of food. When behavioural responses are described, their 417!
interpretation and significance from a welfare perspective is often lacking or 418!
incomplete (Bénard et al 1998, 2006). 419!
The gag or pharyngeal reflex is a reflex contraction of the back of the throat, evoked 420!
by touching the roof of the mouth, the back of the tongue or the back of the throat. 421!
There is a contraction of both sides of the posterior oral and pharyngeal musculature, 422!
and humans report that this is an unpleasant experience (Shriprasad & Shilpashree 423!
2012). The reflex helps to prevent material from entering the throat, except as part of 424!
normal swallowing, and protects against choking and aspiration. There is controversy 425!
as to whether the reflex is present in ducks; we agree with SCAHAW (1998) that it 426!
probably is. Unlike some birds such as pelicans and storks, mulard ducks consume 427!
food by dabbling and sieving and do not swallow large food items. There is no reason 428!
why the pharyngeal reflex would be absent in these ducks. Initially, force-feeding 429!
stimulates this reflex but after a certain time it stops. The adaptation time required for 430!
the gag reflex to be extinguished, and how this affects the duck, are not known. 431!
Carrière et al (2006) compared the behaviour of force-fed mulards (during the hour 432!
after the second, twelfth and twenty-fourth meal) with controls that were kept in the 433!
same conditions but not handled or force-fed. Test birds were force-fed twice daily for 434!
13 days (the amount fed and whether it increased day by day are not specified) while 435!
control ducks had ad-libitum access to food, which was provided every morning at the 436!
same time as the test ducks were force-fed. The behaviour of the control ducks was 437!
video-recorded the day after the recording of the test ducks. 438!
Force-fed ducks spent more time lying down, and walked less frequently and for a 439!
shorter time than control ducks. The authors explain these results by the negative 440!
effects of the duck’s weight gain on posture and movement. We argue that this has 441!
consequences for the duck’s welfare. Excess weight can reduce the animal’s mobility 442!
in a number of ways including pressure from an enlarged abdomen, reduced 443!
respiratory capability and joint pain. As with broilers (Bradshaw et al 2002; Weeks 444!
2014), lack of mobility is likely to lead to further consequences that reduce welfare 445!
such as poor muscle strength, skeletal defects, skin lesions and altered social 446!
interactions with conspecifics. Other changes in behaviour in test birds included 447!
spending less time with their head at rest, reduced grooming and preening, and 448!
spreading their wings and shaking their tail less often. Self-grooming, preening and 449!
wing-stretching are all behaviours generally associated with good welfare in birds 450!
(Rodenburg et al 2005). The time spent performing these behaviours was reduced in 451!
force-fed compared with control birds and decreased over time. Force-fed birds shook 452!
their heads more than controls, especially after the first force-fed meal but also after 453!
subsequent meals. The authors suggest that this may be a reaction to handling by the 454!
force-feeder, or to the introduction of a large amount of food into the oesophagus. 455!
Head-shaking normally indicates an aversive event and also occurs when birds are 456!
deprived of access to open water (Rodenburg et al 2005). It may also be evidence of 457!
stimulation of the gag reflex. 458!
Most intensive farms for foie gras production have air ventilation systems to keep 459!
ambient temperatures relatively low, in an attempt to reduce thermal stress in the birds. 460!
Nevertheless, the force-fed ducks spent a lot of time panting and this increased with 461!
time. After the twelfth meal 5 out of 9 ducks panted, and after the last all panted in the 462!
hour after force-feeding. This behaviour was not evident in the control ducks at any 463!
time. Force-feeding disrupted the test birds’ thermal homeostasis, causing them to 464!
spend a proportion of their time budget panting, while control birds fed ad-libitum 465!
remained in thermal homeostasis and did not pant. These behavioural changes 466!
indicate poorer welfare in the test birds, which worsened over time. Panting to aid 467!
evaporative cooling is part of the thermoregulatory response to the ingestion of large 468!
amounts of high-energy food, as is immersion of the face and, by wet preening, the 469!
body in water (Rodenburg et al 2005). The birds had access to water but it is not clear 470!
whether it was to water troughs, showers, baths or nipple drinkers; it seems that water 471!
was only available for drinking. This study was limited to studying birds for one hour 472!
after each force-feeding and did not consider the effect of handling of test birds, 473!
separate from the effect of force-feeding, as controls were not handled prior to feeding. 474!
Ducks’ behavioural responses to force-feeding were also examined by Faure et al 475!
(1998, 2001). In the first experiment (Faure et al 1998), the hypothesis was that if 476!
force-feeding caused aversion, the ducks would not spontaneously leave their rearing 477!
pen or go into the test pen where they were force-fed. Force-fed birds showed 478!
aversion to entering the test pen, compared with controls (not force-fed). However, 479!
there were some methodological issues with this experiment (eg birds were fed just 480!
once daily). 481!
In the second experiment (Faure et al 2001), the flight distances of ducks from the 482!
force-feeder and from an unknown observer were measured in ducks housed in 483!
individual cages. Flight distance was the distance between the person and the duck’s 484!
cage, at the time when the duck withdrew its head as the person approached it. Tests 485!
were performed several hours after the force-fed meal on days 3, 7, 9 and 11. Initially 486!
the flight distances were similar, but on days 7 and 9 ducks avoided the unknown 487!
person more than the force-feeder and their avoidance of the force-feeder decreased 488!
during the force-feeding period. The authors concluded that there was no evidence of 489!
an aversion to the force-feeder. This is a poorly controlled experiment with alternative 490!
explanations for the results and it does not demonstrate that force-feeding is not 491!
aversive to ducks. It is well known to those who force-feed ducks that the birds show 492!
initial avoidance and struggling but reduce this over time, presumably because they 493!
learn that they are less likely to be caused pain if they do. There is the confounding 494!
effect of greater familiarity of the force-feeder compared with the unknown observer, 495!
and the choice of flight distance as a measure of aversion is problematic (eg duck 496!
movements in an individual cage are limited). Repeating this experiment using two 497!
persons of equal familiarity, with one doing the force-feeding and the other not, as 498!
well as using measures other than flight distance, is indicated. 499!
Effects on physiology 501!
A number of studies have examined the effects of force-feeding and its different 503!
components (handling, intubation) on various physiological indicators of acute and 504!
chronic stress in mulard ducks (Guémené et al 2001; Mirabito et al 2002c; Guémené 505!
et al 2006a; Flament et al 2012; Mohammed et al 2014). Some have shown no effects 506!
of force-feeding on blood corticosterone levels or ACTH sensitivity (eg Guémené et 507!
al 2001; Flament et al 2012), while others have had different results. For example, 508!
Mirabito et al (2002c) found that force-feeding caused significant increases in blood 509!
corticosterone in some ducks on some days and Mohammed et al (2014) noted that 510!
blood corticosterone levels of force-fed ducks rose while those of controls did not. In 511!
humans (Legler et al 1982) and animals (Broom & Johnson 2000) plasma 512!
glucocorticoid concentrations are not consistently related to eating. 513!
The experimental design of studies needs to be improved, and the methodology 514!
clearly established, before the usefulness of corticosterone as a measure of acute or 515!
chronic stress in force-fed ducks can be determined. 516!
Effects on thermoregulation 518!
Force-fed ducks are susceptible to thermal stress, which causes panting in order to 520!
disperse the extra heat generated from digestion. They may spend large amounts of 521!
time, standing or lying down, performing this behaviour (Carrière et al 2006). 522!
Thermal stress makes the duck prone to discomfort, reduces food digestibility and 523!
increases mortality. Nutritional supplements containing electrolytes and anti-oxidants 524!
have been developed to mitigate these effects (Mathiaud et al 2013). Immersion in 525!
water is another homeostatic mechanism for thermoregulation in birds, but if 526!
sufficient water for immersion is not available, heat stress becomes a greater risk 527!
(Rodenburg et al 2005). 528!
Alternatives to force-feeding 530!
Researchers and farmers are keen to find a way of producing foie gras without the 532!
need to force-feed. The main methods are summarised in Guy et al (2007). One 533!
approach is to stimulate the birds to over-eat voluntarily to a degree that is sufficient 534!
to cause hepatic steatosis. Spontaneous over-eating leading to liver steatosis can be 535!
stimulated in geese by manipulating day length (because photoperiod is a major 536!
environmental factor controlling migration and the pre-migratory fattening process) 537!
and feeding regimes (Fernandez et al 2013; Guy et al 2013; Bonnefont et al 2015; 538!
Fernandez et al 2015). However this response is not seen in ducks, the variability in 539!
the response is high, the production cycle is long (up to 31 weeks), the liver produced 540!
is less liked by some consumers (Fernandez et al 2015) and there are negative effects 541!
on the environment (Brachet et al 2015). Life Cycle Analysis (LCA) examines a 542!
product's complete life cycle from raw materials to final disposal of the product 543!
(Williams 2009). Brachet et al (2015) used LCA to estimate potential impacts on the 544!
environment, and found that non force-fed geese had a greater impact due to a longer 545!
production time and higher food consumption while achieving lower liver weights.!546!
EU Regulations 1538/91 and 543/2008 state that in order to be called foie gras, the 547!
minimum liver weight must be 300 grams net in ducks and 400 grams net in geese. 548!
These weights cannot be achieved without force-feeding but if they were reduced, it 549!
may be possible to produce a fatty liver that is still acceptable to consumers without 550!
force-feeding. A maximum liver weight should be specified, in order to prevent the 551!
accumulation of toxic substances and other adverse effects on welfare due to liver 552!
Individual and group housing 557!
Until recently, most production systems placed ducks in individual cages during the 559!
force-feeding period. The cages prevent the ducks from avoiding the force-feeding. 560!
The main advantages to the producer are that the ducks can be force-fed rapidly one 561!
after the other, without the feeder having to catch them, and that “they always remain 562!
in the right position” (Guémené & Guy 2004). Individual cages are small and greatly 563!
restrict the bird’s movements; they do not allow the bird to turn around, stretch and 564!
flap its wings, stretch to its full height or length or show more than a minimal 565!
behavioural repertoire. The degree of restriction increases as the bird grows rapidly 566!
and fattens. 567!
As of January 2016, the individual caging of ducks for foie gras production is illegal 568!
in France (Anon 2015). Ducks have to be housed in groups of at least 3 birds although 569!
cage dimensions and bird density are not specified. This bylaw refers to the Council 570!
of Europe (1999) recommendations for muscovy ducks (Cairina moschata) and 571!
hybrids of muscovy and domestic ducks (Anas platyrhynchos), which state in more 572!
detail what the birds should be able to do when housed together. 573!
Factors that affect welfare in group housing include group size, stocking density, type 574!
of flooring, provision of litter or bedding material, access to water for drinking, and 575!
the provision of water for bathing or at least full immersion of the head (Mirabito et al 576!
2002a, b, c; Mirabito 2006). Management of the air space and ventilation, maintaining 577!
cleanliness and controlling disease, and ensuring homogeneity of groups are also 578!
important. Potential undesirable effects of group housing include increased aggression 579!
between birds, difficulty in maintaining cleanliness (especially in larger groups), 580!
competition at water sources, and difficulties in catching birds causing repeated stress 581!
(Guémené et al 2002; 2006a). 582!
Previous work on group housing has examined the effects of floor space and group 583!
size on production, behaviour and blood corticosterone (Mirabito et al 2002a, b, c). In 584!
general, the best production results were obtained when ducks had 2000 cm2 of floor 585!
area each, and larger groups (9 ducks) had higher mortality and poorer cleanliness 586!
(Mirabito et al 2002a). However, birds kept at the highest stocking density in the 587!
smallest group had more humeral lesions at slaughter, perhaps a reflection of reduced 588!
activity and subsequent bone weakness. Surface area per bird was the main factor that 589!
influenced behaviour, with birds kept at 1000 cm2 each moving less and stretching 590!
their wings less frequently than birds kept at a density of 1500 or 2000 cm2 (Mirabito 591!
et al 2002b). 592!
The effects of group size (3, 6 or 9 ducks) and surface area per bird (1000, 1500 and 593!
2000 cm2) on blood corticosterone before and after force-feeding and on the HPA axis 594!
were explored, and compared with birds housed individually (Mirabito et al 2002c). 595!
Effects of different housing conditions on blood levels of corticosterone were not 596!
clear-cut, and were difficult to interpret. Increases were noted for ducks housed 597!
individually after the 1st and 11th meal, findings which are not in agreement with those 598!
of Guémené et al (2001). There was no evidence of abnormalities in sensitivity or 599!
reactivity of the HPA axis, except for some unusual results obtained for the group of 6 600!
ducks kept at 1500 cm2 stocking density. 601!
Between 2007 and 2009, trials of group versus individual housing of ducks were 602!
performed by Litt (2010). The focus was largely on production outcomes rather than 603!
on welfare. While birds were fed the same amount, group-housed birds had smaller 604!
livers, force-feeding took longer and more water was required for cleaning. There was 605!
a small increase in breast tissue (‘magret’), also noted by Mirabito et al (2002a). 606!
Cage design in group housing 608!
More recent models of group cages have been modified, particularly with regard to 610!
containment (restraint using one or more crowd-gates, ‘peigne de contention’) of birds 611!
when force-fed and the work conditions of force-feeders. The restraining containment 612!
method aims to make force-feeding easier by bringing birds to the front of the cage 613!
and immobilising them. A back wall pushes the birds forwards. As they collect at the 614!
front, the front vertical grid wall descends backwards over them and prevents them 615!
from escaping or moving the body. Group-housed birds may be susceptible to injury 616!
resulting from getting caught in the cage’s containment mechanism, or from being 617!
restrained for a long time as the force-feeder works up one row of cages and back 618!
down the other before releasing the mechanism. Because birds immobilised by the 619!
crowd-gates may be facing any direction, the force-feeder must be able to insert the 620!
feeding tube from any angle (Cepso 2013). This can increase the risk of injury, 621!
especially if the bird struggles and resists or if others get in the way. It is more 622!
difficult and takes longer for the force-feeder to carry out their task, especially with 623!
larger groups (Mirabito et al 2002a; Litt 2010). The force-feeder is unable to develop 624!
a steady rhythm, working their way uninterrupted along a row of cages as is possible 625!
with individual caging. 626!
A brochure by the agricultural group Centre d’Etudes des Palmipèdes du Sud Ouest 627!
Cepso Chambagri (Cepso 2013) illustrates 12 different types of cages available, and 628!
provides a summary table which compares the cage systems with regard to density, 629!
minimum floor space per bird and other parameters. Recommended cage floor surface 630!
area is 4000 cm2 for 3 ducks, 5000 cm2 for 4 and at least 1200 cm2 surface area per 631!
bird (the equivalent of 2 size A4 sheets of paper) for 5 ducks or more. The cage 632!
should be tall enough for the bird to stretch fully to its vertical height and there is 633!
usually no roof. Ten of the systems have a movable back wall, and all but one have a 634!
front vertical grid wall that can move back and down to immobilise the birds. Based 635!
on available published studies, the choice of cage floor surface area per bird seems to 636!
be a compromise between economics and duck comfort (1000-1200 cm2 or 1500-637!
2000 cm2). Most cages are small, with a surface area of 1200 cm2 to 1300 cm2 per bird. 638!
Flooring and provision of litter or bedding 640!
Force-fed ducks are usually kept on a mesh floor (‘caillebotis’) made of some type of 642!
steel (galvanised or stainless) and less commonly of plastic. As force-feeding 643!
progresses, they become more inactive and rest on this firm bare surface as litter or 644!
bedding is not provided. Contact dermatitis is common and develops early during the 645!
production process (Litt et al 2015c). It is already of moderate to marked severity 646!
when birds are ready for force-feeding (end of stage 2b). Lesions may improve, 647!
worsen (Litt et al 2015b) or stay the same (Litt et al 2015a, c) during force-feeding. 648!
Bénard et al (2006) noted that force-fed birds kept on wire mesh floors developed 649!
signs of tibio-tarsal arthritis as well as skin calluses on their feet. These lesions 650!
disappeared when birds were returned to straw litter for free-feeding. 651!
Many environmental factors have been associated with the development of contact 652!
dermatitis in chickens kept for meat production. Why it occurs in some flocks and not 653!
in others is not fully understood. A major contributing factor, particularly at the onset, 654!
is the type of litter, or ground quality if litter is not provided. Damage occurs to the 655!
skin surfaces that have prolonged contact with litter, usually starting with the footpad 656!
and toes, then the rear surface of the hock and, when severe, the breast area. While 657!
high moisture litter is sufficient to cause the condition, litter depth, ammonia levels, 658!
climatic conditions, condensation, ventilation, stocking density, rearing system, leg 659!
weakness, overweight and inactivity, ground quality and diet (such as levels of 660!
methionine, choline and certain vitamins) are also recognised as causative factors 661!
(Haslam et al 2007; Bassett 2009; Shepherd & Fairchild 2010; Hepworth et al 2011; 662!
Saraiva et al 2016). 663!
Council of Europe recommendations (Council of Europe 1999) state that “Where 664!
ducks are housed, floors shall be of a suitable design and material and not cause 665!
discomfort, distress or injury to the birds. The floor shall include an area sufficient to 666!
enable all birds to rest simultaneously and covered with an appropriate bedding 667!
material” (article 10, point 6) and “Adequate litter shall be provided and maintained, 668!
as far as possible, in a dry, friable state in order to help the birds to keep themselves 669!
clean and to enrich the environment” (article 11, point 4). Despite these 670!
recommendations, currently the standard group cage lacks an area where ducks can 671!
rest together, and there is no bedding material or litter to ensure their comfort and 672!
cleanliness or to provide substratum for foraging and exploratory behaviours. The 673!
cage is barren and not enriched beyond the provision of water troughs and 674!
Access to water 677!
Ducks spend considerable time performing complex preening behaviours (Rodenburg 679!
et al 2005). After feeding followed by bathing (an important element being immersion 680!
of the head and wings), they carry out a variety of shaking movements to remove 681!
water and cleaning movements to remove foreign bodies. An elaborate sequence is 682!
then carried out to distribute oil on the feathers from the uropygial gland above the 683!
tail. This is necessary for waterproofing and heat regulation. A short period of sleep 684!
often follows preening. The sequence of feeding, bathing, preening and sleeping may 685!
be repeated a number of times during the day. Council of Europe recommendations 686!
(Council of Europe 1999) state that “Access to an outside run and water for bathing is 687!
necessary for ducks, as water birds, to fulfill their biological requirements. Where 688!
such access is not possible, the ducks must be provided with water facilities sufficient 689!
in number and so designed to allow water to cover the head and be taken up by the 690!
beak so that the duck can shake water over the body without difficulty. The ducks 691!
should be allowed to dip their heads under water” (article 10, point 2). 692!
The provision of a good open water system such as troughs improves eye, nostril and 693!
feather condition and reduces disease (Knierim et al 2004; Jones et al 2009; Jones & 694!
Dawkins 2010a, b; O’Driscoll & Broom 2011; O’Driscoll & Broom 2012, Liste et al 695!
2012). Water troughs must be wide enough and deep enough so that ducks can 696!
immerse and wet their head fully, and long enough so that there is no competition 697!
between ducks for access although it may not be necessary for all birds to bathe 698!
simultaneously (Waitt et al 2009). The Cepso brochure (Cepso 2013) states that there 699!
should be at least 800 mm length of water trough per cage, but it is not clear if this is 700!
dependent on group size. In addition, the width and depth dimensions of the troughs 701!
are not supplied. While studies state that water troughs are provided for drinking and 702!
head immersion, to our knowledge none published so far have examined whether the 703!
troughs are actually used for what they are intended, or reported on water cleanliness 704!
and duck behaviour at the troughs. 705!
Dimensions are available for troughs used in experimental conditions in British 706!
studies of farmed ducks, eg: 950 mm long, 125 mm wide and 80 mm deep (Jones et al 707!
2009; Waitt et al 2009) or 1600 mm long, 150 mm wide and 100 mm deep 708!
(O’Driscoll & Broom 2011, Liste et al 2012, 2013). However, ducks in these studies 709!
are younger, smaller and lighter than ducks at force-feeding, and the troughs are often 710!
placed on the ground rather than attached to cages. Little attention seems to have been 711!
paid to water trough dimensions in other studies, or to whether the birds are able to 712!
perform immersive behaviour in addition to drinking, or to water cleanliness and 713!
trough maintenance. As ducks lack sweat glands, immersion in water as well as 714!
panting is a vital homeostatic mechanism for thermoregulation in force-fed birds 715!
subjected to a high level of thermal stress due to the ingestion of large amounts of 716!
When mulard ducks are kept in individual cages, they have access to water via nipple 718!
drinkers (Rodenburg et al 2005) or via troughs but, because of the restrictive cage, the 719!
type of trough and increasing bird size, they may not be able to immerse their heads 720!
fully, spread water over their feathers and self-groom. It is notable that they are 721!
unable to keep themselves clean, especially towards the end of force-feeding. Force-722!
feeding with maize mash is messy and it not clear whether group housing results in 723!
cleaner birds with improved welfare. 724!
Other welfare issues 726!
The human-animal relationship 728!
In the case of foie gras production, the relationship between the stockman (the force-730!
feeder) and the force-fed ducks has received little attention despite the major impacts 731!
stockmanship has on animal welfare (Boivin et al 2003; Hemsworth 2007). Perhaps 732!
this is because the force-feeder is often only involved in the final stage rather than in 733!
the whole production process, and their work is normally restricted to force-feeding 734!
and cleaning activities. Concerns have been raised that group housing (obligatory as 735!
of January 2016) makes the force-feeder’s work harder and take longer (Litt 2010). 736!
Workers have to modify their technique and movements, and access to birds is more 737!
Fear responses in ducks include freezing, alarm calling, agitation, attempts to run 739!
away rapidly and vigourous struggling if caught (Ekesbo 2011). There is substantial 740!
evidence that negative interactions between humans and animals increase the animals’ 741!
fear (Boivin et al 2003; Hemsworth 2007); fearful animals are more difficult to 742!
handle. Mulards show fear of humans (Arnaud et al 2008), and when force-fed they 743!
pull back (‘movement de recul’) (Laborde & Voisin 2013). Difficulties in catching 744!
and restraining birds for force-feeding led to the development of a containment 745!
system using a crowd-gate, which reduces the birds’ ability to struggle, resist or 746!
escape. The need for containment strongly indicates that ducks find the force-feeding 747!
procedure aversive. 748!
Domestic animals usually develop a relationship with the person looking after them, 749!
especially if that person provides food and other positive resources such as bedding, 750!
and activities such as talking, petting and grooming. Containment may make force-751!
feeding quicker and easier, but has a negative impact on the stockperson-animal 752!
relationship. If ducks were being offered appropriate food and did not find the 753!
procedure painful, frightening or otherwise aversive, there would be no need for 754!
containment. Instead, they would move voluntarily towards the force-feeder and stay 755!
still while being fed because food is a necessary and desirable resource supplied by 756!
the feeder. Habituation is defined as a decrease in responding resulting from repeated 757!
stimulation (Shettleworth 2010), providing that it is not due to sensory adaptation or 758!
motor fatigue. Habituation to an extremely unpleasant stimulus is less likely than to a 759!
slight one, and is also unlikely if the stimulus remains biologically relevant 760!
(Shettleworth 2010). Habituation to force-feeding is unlikely to occur. 761!
Control over the environment and motivation 763!
A major objection to the practice of foie gras production is that the birds cannot chose 765!
what, when and how much they will eat. They cannot show a food preference or feed 766!
spontaneously. They are the only farmed species that is not able to feed by expressing 767!
normal feeding behaviour, and are fed considerably more than they would eat 768!
voluntarily. They receive this food without having the possibility to forage in a 769!
species-specific manner ie by pecking, nibbling and swallowing and, if there is access 770!
to open water, dabbling, sieving and up-ending. 771!
Motivated behaviours have two phases: an ‘appetitive’ phase in which the animals 772!
search or prepare for the opportunity to perform a ‘consummatory’ phase (Mason & 773!
Burns 2011). In the case of food, their expression is vital to the animal’s survival so 774!
both phases are driven by strong motivations, and emotions appear to be important in 775!
their control. Being unable to satisfy these strong motivations leads to frustration 776!
(Mason & Burns 2011). 777!
An important concept in relation to understanding animal welfare is the control which 778!
an individual has over its environment (Broom 1991). Welfare is poorer when the 779!
individual lacks control and is affected by the consequences (Broom 2008). Birds in 780!
foie gras production cannot control their own feeding nor can they control the amount 781!
and nature of their contact with humans. This lack of control leads to very poor 782!
The European Charter and the Welfare Quality® project 785!
In 2008 the European Federation of Foie Gras, consisting of all the representatives of 787!
foie gras producing countries in the European Union, was signatory to a European 788!
Charter on the “breeding of waterfowl for foie gras” (see 789!
http://www.eurofoiegras.com/docs/EUROFOIEGRAS_CHARTE_UK.pdf). (The 790!
term ‘élevage’ is not translated accurately here; the Charter is not about breeding but 791!
about rearing and fattening, or production). The Charter is derived from the twelve 792!
criteria of the Welfare Quality® project and uses the term ‘assisted feeding’ in the 793!
English and ‘gavage’ in the French version. The Federation claims that “if performed 794!
by professionals under regulated conditions, gavage does not cause any suffering to 795!
the animals” (see http://www.eurofoiegras.com/en/page/euro-foie-gras_p134/). A 796!
support programme called ’Palmi G Confiance’ was created in 2014 to help foie gras 797!
producers meet the standards of the European Charter with regard to animal welfare 798!
and good practice. Researchers are working with the poultry industry to develop a 799!
simple welfare assessment method that can be used on a large scale and is largely 800!
based on animal measures. Some research is focussed on identifying measures easily 801!
taken in the abattoir that are correlated with on-farm measures that are more difficult 802!
to collect (Litt et al 2015a). 803!
The four welfare principles and 12 criteria proposed by the Welfare Quality® project 804!
(Welfare Quality® Consortium 2009) are a development of the Five Freedoms 805!
(Brambell 1965). We have made a preliminary attempt at assessing the welfare of 806!
ducks in foie gras production using the Welfare Quality® assessment system (Table 807!
1). There are four columns in the Welfare Quality® assessment system. The first lists 808!
the four welfare principles, and the second presents the criteria associated with each 809!
of these principles. Using the information provided by this review, we have completed 810!
the last two columns. In the third column we state whether the criterion is met or not, 811!
and in the fourth we give examples of how the criterion is or is not met. We conclude 812!
that only three of the 12 criteria and none of the welfare principles are met in current 813!
systems of foie gras production. 814!
Table 1 at end of paper 815!
Other stages of foie gras production 817!
While the primary aim of this review has been to highlight the welfare problems in 819!
the last stage of foie gras production, welfare problems have also been identified in 820!
the first two stages. These include the early, frequent and rapid development of 821!
contact dermatitis, fear of humans and high sensitivity to the environment, and lack of 822!
access to open water for bathing or at least full immersion of the head. It seems that 823!
under commercial conditions water is normally only provided by nipple drinkers, 824!
despite ducks being aquatic animals who spend most of their lives close to or on water. 825!
Conclusions and animal welfare implications 827!
Force-fed birds are the only farmed species that is not able to feed by expressing 829!
normal feeding behaviour. There is substantial evidence from behavioural 830!
observations that force-feeding is aversive, and causes high mortality compared with 831!
other duck production systems. 832!
The physical condition of the birds deteriorates as they progress through the stages of 833!
foie gras production. Force-feeding an unbalanced diet in large amounts causes 834!
significant liver pathology. Hepatic steatosis has the potential to be fatal if force-835!
feeding is prolonged beyond 15 to 16 days. Force-feeding causes oesophagitis and 836!
leads to other abnormalities such as gait disturbances, wing lesions, and bone 837!
pathology which can result in fractures. Contact dermatitis, a painful skin condition, is 838!
widespread, starts in the early stages of production, is present in all stages and can be 839!
Due to their fear of humans, nervousness and sensitivity to the environment, mulard 841!
ducks are maladapted to the conditions of foie gras production, especially during 842!
force-feeding. When group-housed they keep away from the force-feeder; they have 843!
to be rounded up and immobilised with crowd-gates in order to be force-fed. This 844!
indicates that ducks regard the experience of being handled and force-fed as a 845!
negative one, to be avoided. They are very susceptible to thermal stress due to the 846!
large amounts of food force-fed, and this makes them spend a large proportion of their 847!
time panting. 848!
Housing provisions are poor, with small, barren group cages and a bare mesh floor; 849!
resting places, litter or bedding are not provided despite Council of Europe 850!
recommendations. It is not clear whether the troughs supplied on the cages of force-851!
fed ducks are effective for bathing or full head immersion, or enable them to keep 852!
their plumage clean and to thermoregulate adequately In the first two stages of 853!
production, access to open water suitable for bathing may be lacking; water supplied 854!
in the form of nipple drinkers does not allow full immersion of the head. 855!
The European Federation of Foie Gras claims that “if performed by professionals 856!
under regulated conditions, gavage does not cause any suffering to the animals.” We 857!
conclude from this literature review that force-feeding causes very poor welfare in 858!
ducks and should not be practised. In the future, the production of foie gras in ducks 859!
without the need to force-feed may become possible. In order to prevent the 860!
accumulation of toxic substances and other adverse effects on welfare due to liver 861!
malfunction, maximum liver weights should be specified and based on scientific 862!
studies. To avoid poor welfare associated with inadequate housing and management, 863!
birds should be checked before and after slaughter using animal-based welfare 864!
outcome indicators. For example, maximum acceptable prevalences of contact 865!
dermatitis, posture and walking difficulties, wing fractures and other body lesions 866!
could be established. 867!
Acknowledgements and conflicts of interest 869!
We are very grateful to Dr D. Guémené of INRA and to Dr J. Litt of ITAVI, who 871!
provided us with references and were very helpful in answering our questions. We 872!
should like to thank the Belgian charity GAIA for supporting the writing of this report 873!
at the University of Cambridge, and Mr. Adolfo Sansolini for his encouragement and 874!
help. Thanks are also due to two anonymous reviewers for their constructive 875!
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Table 1. Principles and criteria that underpin the Welfare Quality® assessment system, 1!
and whether they are met by force-feeding of mulard ducks 2!
Example of how criterion is or
is not met
Animals should not suffer
from prolonged hunger, ie they
should have a sufficient &
Duck is fed a diet that is
neither appropriate nor
sufficient (diet is excessive); it
cannot regulate its intake to
achieve satiety & homeostasis
Animals should not suffer
from prolonged thirst, ie they
should have a sufficient &
accessible water supply.
There may be problems with
ensuring ease of access to
water troughs & trough design
Animals should have comfort
There is no resting area & no
bedding, the floor consists of
wire or plastic mesh
Animals should have thermal
comfort, ie they should neither
be too hot nor too cold.
There is thermal stress due to
large amounts of high energy
food leading to prolonged
Animals should have enough
space to be able to move
More behavioural research is
necessary to confirm optimal
cage size & design & stocking
Animals should be free of
Injuries due to containment,
capture, handling & force-
Animals should be free of
disease, ie farmers should
maintain high standards of
hygiene & care
Footpad & hock dermatitis,
lesions to breastbone are
frequent & often severe; liver
steatosis is caused deliberately
Animals should not suffer pain
induced by inappropriate
slaughter, or surgical
procedures (eg castration,
Containment, capture, handling
& force-feeding may be
sources of pain; high
prevalence of wing lesions
caused by handling & transport
Animals should be able to
express normal, non-harmful,
social behaviours, eg
Further research needed on
social behaviour in group
housing, optimal group size &
social behaviours, signs of
Animals should be able to
express other normal
behaviours, ie it should be
possible to express species-
specific natural behaviours
such as foraging.
There is no substratum for
foraging; further research is
necessary on the use of water
troughs, preening & grooming
Animals should be handled
well in all situations, ie
Catching, handling & force-
feeding do not promote good
handlers should promote good
poor handling during transport
prior to slaughter causes wing
Negative emotions such as
fear, distress, frustration or
apathy should be avoided
whereas positive emotions
such as security or
contentment should be
Fear, distress, frustration, pain
& other negative emotions are
very likely when ducks are
subjected to the stages of foie
gras production, especially
during force-feeding. Problem
of nervousness & hyper-
reactivity in mulard ducks