Animal Behaviour 77 (2009) 275288

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Animal Behaviour
journal homepage: www.elsevier.com/locate/yanbe

Review

Freedom from hunger and preventing obesity: the animal welfare

implications of reducing food quantity or quality
Richard B. DEath a, *, Bert J. Tolkamp b, Ilias Kyriazakis c,1, Alistair B. Lawrence a
a
Animal Behaviour and Welfare Department, Scottish Agricultural College, Edinburgh
b
Animal Nutrition and Health Department, Scottish Agricultural College, Edinburgh
c
Veterinary Faculty, University of Thessaly

a r t i c l e i n f o
In animals, including humans, free access to high-quality (generally energy-dense) food can result in
Article history: obesity, leading to physiological and health problems. Consequently, various captive animals, including
Received 11 June 2007 laboratory and companion animals and certain farm animals, are often kept on a restricted diet.
Initial acceptance 1 September 2008 Quantitative restriction of food is associated with signs of hunger such as increases in feeding motivation,
Final acceptance 20 October 2008 activity and redirected oral behaviours which may develop into stereotypies. An alternative approach to
Published online 12 December 2008 energy intake restriction is to provide more food, but of a reduced quality. Such alternative diets are
MS. number: RV-74 usually high in bre and have lower energy density. The benets of these alternative diets for animals are
controversial: some authors argue that they result in more normal feeding behaviour, promote satiety
Keywords: and so improve animal welfare; others argue that metabolic hunger remains no matter how the
chicken
restriction of energy intake and weight gain is achieved. We discuss the different arguments behind this
diet
controversy, focusing on two well-researched cases of food-restricted farmed livestock: pregnant sows
feeding behaviour
hunger and broiler breeders. Disagreement between experts results from differences in assumptions about what
nutrition determines and controls feeding behaviour and food intake, from the methodology of assessing animal
obesity hunger and from the weighting placed on naturalness of behaviour as a determinant of welfare.
pig Problems with commonly used behavioural and physiological measures of hunger are discussed. Future
qualitative food restriction research into animal feeding preferences, in particular the relative weight placed on food quantity and
stereotypy quality, would be valuable, alongside more fundamental research into the changes in feeding physiology
associated with alternative diets.
2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Humans and animals exposed to a wide variety of freely avail-
able high-quality foods typically consume excess energy which is
deposited as lipid, resulting in their being described as overweight
or obese (West & York 1998; Lieberman 2006). Food quality
generally refers to energy density of the food, but in this paper we
include other quality aspects, especially the inclusion of appetite
suppressants in broiler diets, under this term. Excessive energy
deposition is an actual or potential problem in captive animals
including companion animals (Bufngton 1994; Hawn 2005;
German 2006), zoo animals (Schwitzer & Kaumanns 2001), labo-
ratory animals (Home Ofce 1989, 2003) and certain farm animals
(Higgins & Anderson 1983; Meunier-Salaun et al. 2001; Mench
2002). It can result in health problems such as diabetes mellitus,
cardiorespiratory disease including heart failure, urinary disorders,
reproductive disorders such as multiple ovulation in broiler
breeders (Hocking et al. 1987), locomotory problems (lameness),
* Correspondence: R. B. DEath, SAC, West Mains Road, Edinburgh EH9 3JG, U.K.
E-mail address: rick.death@sac.ac.uk (R.B. DEath).
1
I. Kyriazakis is at the Veterinary Faculty, University of Thessaly, 43100 Karditsa,
Greece.
tumours and increased mortality (Katanbaf et al. 1989; Hocking
et al. 1996; Fan et al. 2003; Hawn 2005; German 2006). Overweight
animals may also suffer from thermal discomfort (Savory et al.
1993b; Kubkova et al. 2001).
For various captive animals, access to food is restricted to
ensure their body weights are conducive to good health and
reproductive efciency and to avoid obesity. Typically this is
achieved by restricting the quantity of food provided (quantita-
tive restriction), but this can result in hunger, evidenced by
increased motivation for food and increased activity, in particular
foraging behaviour (Epling & Pierce 1988; Lawrence et al. 1993;
Vitousek et al. 2004). Once food is consumed, foraging activity is
redirected towards nonfood substrates and may become stereo-
typic in nature (Rushen 1985; Lawrence & Terlouw 1993; Savory
& Maros 1993). Because of these signs of hunger, quantitative
restriction in captive animals has attracted the interest of animal
welfare pressure groups (CIWF versus Defra 2003, case no. CO/
1779/2003, Queens Bench Division), advisory bodies such as the
Farm Animal Welfare Council (FAWC 1998, recommendation 64)
and legislators (EC Council 2001; Home Ofce 2003; U.K.
Parliament 2006).

0003-3472/$38.00 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2008.10.028
276 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
In response to this concern over the apparent negative animal
welfare consequences of quantitative food restriction (namely
hunger), dietary manipulation has been proposed as an alternative
(reviewed in Meunier-Salaun et al. 2001; Mench 2002; Hocking
2004; Ru & Bao 2004). Where food is reduced in quality, but offered
ad libitum, this is termed qualitative restriction (e.g. Sandilands
et al. 2006). Such diets are an effective means of food restriction
because ad libitum-fed animals consume less energy from low-
quality foods (Brouns et al. 1995; Savory et al. 1996; West & York
1998; Whittemore et al. 2002; Tolkamp et al. 2005; Johnston et al.
2006). Diets where food quality is reduced, but still offered in
a controlled quantity less than the animals desired ad libitum
intake, are called rationed alternative diets (e.g. Zuidhof et al.
1995; Danielsen & Vestergaard 2001; de Jong et al. 2005). Here, we
refer to these two situations (qualitative restriction and rationed
alternative diets) as alternative diets. Such alternative diets
usually involve using foods of lowered quality through the addition
of feedstuffs containing bulky ingredients or dietary bre such as
sugar beet pulp (Whittaker et al. 2000; Danielsen & Vestergaard
2001), wheat bran and cobs (Robert et al. 1997) or oat hulls (San-
dilands et al. 2005), although nonbrous nutrients known to
suppress appetite have also been used in poultry (phenylpropa-
nolamine, Oyawoye & Krueger 1990; monensin sodium, Savory
et al. 1996; calcium proprionate, Savory & Lariviere 2000), some-
times in combination with bre (Sandilands et al. 2005, 2006).
The question of whether alternative diets reduce hunger and so
enhance animal welfare in comparison to quantitative restriction is
controversial, and the reasons behind this controversy are the
subject of the present review. There has been some discussion of
this question in relation to companion animals (Butterwick &
Hawthorne 1998; Umeda et al. 2006), but most research involves
two situations in farmed livestock: broiler breeders (the parent
stock of meat chickens, Gallus gallus domesticus) which are severely
restricted during rearing (2550% of ad libitum intake, Savory et al.
1993b; Renema et al. 2007) and nonlactating (dry) sows, Sus scrofa,
which are restricted during pregnancy (5060% of ad libitum
intake, Lawrence et al. 1988). These two situations are the focus of
this review. Some authors have concluded that welfare of these
species is improved by alternative diets because foraging behaviour
is more normal and characteristics of the food enhance satiety
(Zuidhof et al. 1995; Robert et al. 1997; Zonderland et al. 2004). This
view is reected in policy: in the EU, there has been a requirement
that sows receive a sufcient quantity of bulky or high-bre food as
well as high-energy food since 2001 (EC Council 2001), and this is
implemented in the member states through legislation (e.g. Neth-
erlands, De Leeuw 2004) or codes of practice (e.g. U.K., Defra 2003).
Other researchers have discussed the conicting evidence and
interpretations of the welfare benets of alternative diets (Day et al.
1996; Meunier-Salaun et al. 2001; Mench 2002; Hocking et al.
2004; Ru & Bao 2004; de Jong et al. 2005), while a third group have
argued that there is no evidence of any welfare benets. Their
position is that the hunger indicators of total oral behaviours and
activity remain similar between quantitative restriction and alter-
native diets, and that if nutrient requirements and energy needs
remain unsatised metabolic hunger will occur (Lawrence et al.
1989; Owen 1992; Savory et al. 1996; Dailey & McGlone 1997;
Savory & Lariviere 2000; McGlone & Fullwood 2001).
In this review, we examine in detail the reasons underlying the
controversy over alternative diets. We begin by dening hunger
and discuss some general issues concerning its measurement. We
then highlight the need to compare treatment groups with similar
growth or body weight change when comparing quantitative
restriction with alternative diets. We then review the diverse
indicators used to measure hunger, including behavioural obser-
vations, behavioural tests and physiological indicators. In each case
we assess the value and problems with the indicators used and,
where appropriate, suggest avenues for further research. We
conclude by summarizing what we believe to be the principal
reasons for the controversy and discussing the wider implications
of the review. We believe that our conclusions are of interest to
pure and applied animal behaviour scientists and also to scientists
from other elds of inquiry interested in the question of how we
assess hunger and its wider effects.
DEFINING HUNGER
Hunger (or its converse, satiety) is usually not well dened in the
literature (Day et al. 1997). In this paper we dene hunger as
a negative subjective state experienced by an animal that is
chronically undernourished. Some caveats and justications for this
denition are as follows. (1) We emphasize the longer term because
chronic restriction has a much greater inuence on feeding moti-
vation than acute food deprivation does (Savory et al. 1993b; Fer-
guson & Paule 1995, 1997; Bokkers et al. 2004). For example, broiler
breeders fed to around 30% of ad libitum were over three times as
food motivated in an operant task as birds fed ad libitum and then
fasted for 72 h (Savory et al. 1993b). This denition also avoids
confusion with terms related to short-term appetite regulation.
Animals eat until they are satiated (meal ending) and satiety
declines until hunger results in the next meal (meal initiation, e.g.
de Graaf et al. 2004). (2) Animal subjective states are (for us)
a critical component of animal welfare (Dawkins 1990; Duncan
1993; Fraser & Duncan 1998), at least as important as naturalness of
behaviour and functional/health considerations (reviewed in Fraser
et al. 1997). Although animal subjective states cannot be directly
observed, the choice of indirect indicators of hunger should ideally
be assessed by considering their likely relationship with the ani-
mals subjective perception of hunger. (3) The reference to under-
nourishment is somewhat general, side-stepping the issue of which
specic nutrients might be in short supply (e.g. Kyriazakis 1994). In
sows and broiler breeders, diets are mainly designed to restrict
energy intake, so this will be our focus too. The concept of under-
nourishment implies that the animals intake is falling short of its
desired intake. We discuss different theories as to what determines
an animals desired intake target or goal in a later section.
HOW TO MEASURE HUNGER
The question of how to measure animal welfare in general has
been debated and reviewed elsewhere (e.g. Broom & Johnson 1993;
Mason & Mendl 1993; Dantzer 2002; Paul et al. 2005; Botreau et al.
2007), and these discussions are relevant to the assessment of
hunger. For example, Mason & Mendl (1993) described how welfare
measures are typically validated in two ways: (1) by measuring
responses to a situation or stimulus that is thought by the experi-
menter to be aversive (e.g. unavoidable electric shocks, isolation
from a social group), and (2) by analogy with the responses of
humans who report negative emotional states. The rst of these is
often applied to hunger measures, where different levels of quan-
titative restriction are used (rst column in Tables 1 and 2). The
second of these is also relevant, with some researchers making
reference to the human literature in support of their chosen
measures (e.g. De Leeuw 2004). In the literature on feeding systems
for sows and broiler breeders, scientists have made use of indica-
tors used more generally in animal welfare assessment (e.g.
hypothalamicpituitaryadrenal (HPA) axis measures, stereotypy,
measure of motivation such as operant conditioning) as well as
measures that are more specically related to feeding (e.g. ratio of
glucose to nonesteried fatty acids (NEFA), insulin levels, feeding
rate, compensatory feeding; Tables 1 and 2).
To validate indicators of hunger, it is common rst to test the
indicator using various degrees of quantitative restriction (rst
 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288 277

Table 1
Comparisons of broiler breeder behaviour and physiology in different feeding situations

Measurement
Behaviour observed
Meal patterns
Time spent eating
General activity
Total foraging-related oral behaviour
Nonfeeding oral activities (redirected pecking Higher610,12,16,17,22,25
and stereotypy; excludes aggression)
Drinker use (includes observed
pecking at drinkers, observed
drinking and measured water use)
Aggressive behaviour
Comfort behaviour (preening etc.)
Quantitative restriction on
high-quality food, compared to
greater amounts of high-quality
food (up to ad libitum)
Loss of control over initiation and
termination of meals, food provided
at certain times and quickly runs
out21,23
Much shorter9,17,21,24
Higher2,712,14x,16,17,21,22,25
Higher2,8,10,17,21, same at 6 and 12
weeks, higher at 18 weeks7
Higher4,6,7,8,9,21,22,25, lower12
Higher15
Same16, lower2,17
Alternative diets (high bre) compared Alternative diets (nonbre appetite
to quantitative restriction suppressants) compared to quantitative
restriction*
Improved, more normal pattern over 24 h25. Improved, more normal pattern over
More able to choose when to initiate and 24 h25y. More able to choose when to
terminate meals initiate and terminate meals10y
Longer, more normal3,19,25,26z Longer, more normal18,19y
Similarly high10,11**,19,20,25,26z, lower on Similarly high19,20, some
one diet3 reduction18,25
Same18 Higher18/lower19
Same26z, lower on some diets3,10, lower25, Lower25/almost absent18,19
almost absent19
Same10, same during rearing, reduced Drinking increased, water wasted by
during laying26z, reduced, more normal5 pecking at drinker reduced18
d d
Higher5

Behavioural test
Rate of eating Increased24 Lower19 Lower18,19
Compensatory feeding Increased2
Operant responding (soon after meal) Higher20yy,24 Lower20yy Lower20yy
Operant responding (several hours later) Higher1zz,20yy,24 As high20yy As high20yy
Tonic immobility Lower7xx,8,23, same9
Open eld activity Higher2

Physiology
Plasma corticosterone Same9,23, higher below Higher for some feeds (sugar beet pulp), Same18,19***,25
a threshold2,7,12 (50% of ad libitum lower for others (oat hulls)25,
weight), higher6,8,25 Same3,5,19***
Heterophil:lymphocyte ratio Same9,13,22,25, higher6,14,23, higher Reduced at 12 weeks but not at 20 or 50 Same18,19,25
below a threshold7 (50% of ad weeks26z, reduced for 10 or 20% bre
libitum weight), higher at 6 weeks, diets10, same5,11**,19, higher for one
lower at 24 weeks8 feed3,25
Creatine kinase Reduced6, reduced7 (at 12 and 18
weeks), reduced (at 6, 12 and 18
weeks)8, reduced at 60 weeks9
Other plasma enzymes (aspartate Same7, some differences8
transaminase, lactate dehydrogenase,
alkaline phosphatase)
Basophils Same25, lower7,8,23, higher6,13,14 Same11**,19,25, higher for oat hulls and Same19
sunower10
Other white blood cells (monocytes, Same25, monocytes higher, Same11**,12,19,25 Same19,25
eosinophils) eosinophils lower8
Antibody response to challenge (e.g. Same79 Same5,11**
phytohaemagglutinin, sheep red blood
cells7, various poultry viruses19)
Feed passage time and water content of Diet including sugar beet pulp: more
different gut regions water in the jejunum/duodenum10,11**
Glucose/NEFA ratio Higher2 Higher3

Text and references in bold indicate where treatment groups being compared showed similar body weight changes. Sources: (1) Bokkers et al. (2004); (2) de Jong et al. (2003);
(3) de Jong et al. (2005); (4) Hocking (1993); (5) Hocking (2006); (6) Hocking et al. (1993); (7) Hocking et al. (1996); (8) Hocking et al. (2001); (9) Hocking et al. (2002); (10)
Hocking et al. (2004); (11) Jones et al. (2004); (12) Kubkova et al. (2001); (13) Maxwell et al. (1990); (14) Maxwell et al. (1992); (15) Mench (1988); (16) Merlet et al. (2005); (17)
Puteram et al. (2006); (18) Sandilands et al. (2005); (19) Sandilands et al. (2006); (20) Savory & Lariviere (2000); (21) Savory & Maros (1993); (22) Savory et al. (1992); (23)
Savory et al. (1993a); (24) Savory et al. (1993b); (25) Savory et al. (1996); (26) Zuidhof et al. (1995).
* Sandilands et al. (2005) and one of the treatments in Sandilands et al. (2006) involved a diet combining high-bre and appetite suppressant ingredients. These ndings are
reported under the nonbre appetite suppressants column. Results relating to other nutritional manipulations (e.g. low-protein diets in Sandilands et al. 2006) have been left out.
y
The effect on meal patterns, rate of eating and time spent eating depends on the diets offered. When alternative diets are offered ad libitum (qualitative restriction), the
chickens control the meal pattern. When modied quantitative restriction is used, eating rate is slower and eating time longer, but meal patterns are controlled to a greater
extent by the time of food delivery. There is a continuum between these depending on the quality and quantity of diet offered.
z
In Zuidhof et al. (1995), all birds were quantitatively restricted to achieve the desired growth curve, with 15% or 30% oat hulls added, so changes are generally less marked
than in other studies with more generous quantities of bre.
x
The relationship between feeding level and sitting was curvilinear in Maxwell et al. (1992). Sitting peaked at 70% of ad libitum. As restriction became more severe from 70
to 25% of ad libitum, sitting was reduced. However, it also declined from 70 to 90 and 100% of ad libitum perhaps because these animals were standing to try to lose heat.
** Unusually, high-bre diets in Jones et al. (2004) contained considerably more fat than conventional diets to equalize metabolizable energy (ME) per kg between different
diets. Equal weights of conventional and high-bre diets were then fed.
yy
Savory & Lariviere (2000) found signicant effects of diet type (including quantitative and qualitative restriction) on operant responding for food, but when body weight
was tted as a covariate there were no differences, suggesting that for birds of similar weight the type of diet did not affect feeding motivation.
zz
Bokkers et al. (2004) used broilers rather than broiler breeders, but they were fed at similar levels of restriction to broiler breeders.
xx
Hocking et al. (1996) used time to rst head movement rather than time to stand following tonic immobility, arguing that the latter could be confounded by agility
differences between light and heavy birds.
*** In Sandilands et al. (2006), plasma corticosterone was higher in one treatment where growth was most severely depressed, but there was no difference between birds fed
quantitative and qualitative restriction diets that led to similar growth.
278 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288

Table 2
Comparisons of dry sow behaviour and physiology in different feeding situations

Measurement Quantitative restriction on high-quality Alternative diets (high-bre) compared to quantitative restriction
food, compared to greater amounts of
high-quality food (up to ad libitum)
Behaviour observed
Meal patterns Loss of control over initiation and Normal. Animal chooses when to initiate and terminate
termination of meals, food provided bouts of eating (meals)6*
at certain times and quickly runs out28,4
Rate of eating Increased28 Normal/slower3,5,2022,24,27*
Time spent eating Much shorter3,28 Normal/longer3,4,6,8,13,17,19,20,2224,26,30,31*
General activity Higher1,2y,3,9,28 Higher13/Same as17,23,25,26,30/lower than quantitative
restriction3,6,11,12,2022,24,25,31,32, lower late in the day10
Total foraging-related oral behaviour Higher3,9 Same as20,30,31/lower than quantitative restriction6,11
Nonfeeding oral activities (redirected Higher1,2y,3,9,28 Remain similar12,13,26z,30/lower level 3,6,8,11,17,2022,25,26z,29,31,32
foraging and stereotypy; excludes aggression)
Drinker use Higher28 Same20,26,30, lower6,22,25,31
Aggressive behaviour Higher31, lower8 (fewer skin lesions)17

Behavioural test
Operant responding (soon after meal) Higher1416,26 Higher16x, same21, lower26
Operant responding (several hours later) Higher14,15 Same16,21,26

Physiology
Cortisol Higher peak following meal, baseline similar27,
no difference 5 h postfeeding13
Glucagon Same premeal22
Insulin Postfeeding peak lower7,10,22,27 and delayed10,22, same
premeal7,10,22, more stable over time10
Glucose Postfeeding peak lower7,10,22,27 and delayed10,22, same
premeal7,10,22, more stable over time11
Acetate Higher premeal, remaining higher and more constant postmeal7
Nonesteried (free) fatty acids Same27, same premeal22
Volatile fatty acids Higher19
Cholesterol Lower19
Heart rate Lower baseline26 Lower rise in response to food arriving26
Gastrointestinal transit time Lower19
Water content of faeces Higher19
Neutrophil:lymphocyte ratio, mitogen-induced Same18
lymphocyte proliferation, natural killer cell
toxicity, neutrophil chemotaxis

Text and references in bold indicate where treatment groups being compared showed similar body weight changes. Sources: (1) Appleby & Lawrence (1987); (2) Bergeron &
Gonyou (1997); (3) Bergeron et al. (2000); (4) Brouns & Edwards (1994); (5) Brouns et al. (1992); (6) Brouns et al. (1994a); (7) Brouns et al. (1994b); (8) Danielsen & Vestergaard
(2001); (9) De Leeuw & Ekkel (2004); (10) De Leeuw et al. (2004); (11) De Leeuw et al. (2005b); (12) Fraser (1975); (13) Holt et al. (2006); (14) Lawrence & Illius (1989); (15)
Lawrence et al. (1988); (16) Lawrence et al. (1989); (17) Martin & Edwards (1994); (18) McGlone & Fullwood (2001); (19) Mroz et al. (1986); (20) Ramonet et al. (1999); (21)
Ramonet et al. (2000a); (22) Ramonet et al. (2000b); (23) Ramonet et al. (2000c); (24) Rijnen et al. (2003); (25) Robert et al. (1993); (26) Robert et al. (1997); (27) Rushen et al.
(1999); (28) Terlouw et al. (1991); (29) van der Peet-Schwering et al. (2003b); (30) Whittaker et al. (1998); (31) Whittaker et al. (1999); (32) Zonderland et al. (2004).
* The effect on meal patterns, rate of eating and time spent eating depends on the diets offered. When alternative diets are offered ad libitum (qualitative restriction), the
sows control the meal pattern. When modied quantitative restriction is used, eating rate is slower and eating time longer, but meal patterns are controlled to a greater extent
by the time of food delivery. There is a continuum between these depending on the quality and quantity of diet offered.
y
Bergeron & Gonyou (1997) does not strictly t into any of the columns here. They provided sows with more energy through an energy-dense food (rather than greater
quantities of their usual diet) and found reduced activity and stereotypy in comparison to a conventional (quantitative restriction) diet.
z
In Robert et al. (1997), one of the high-bre treatments reduced postmeal stereotypy relative to quantitative restriction, the other only tended to.
x
In Lawrence et al. (1989), the quantitative restriction groups had nished their feed at the time of the rst operant test, but animals on qualitative restriction had not. This is
likely to account for their higher operant responding for food rewards.

column in Tables 1 and 2), and then to apply this measure to
compare alternative diets with quantitative restriction. Sometimes
both approaches are combined into one experiment (e.g. Lawrence
et al. 1989; Savory et al. 1996; Bergeron et al. 2000; Savory & Lar-
iviere 2000). On the face of it, this seems sensible, but can be
problematic in practice. For example, to assess various measures of
hunger, de Jong et al. (2003) fed broiler breeders at various degrees
of quantitative food restriction. Indicators that varied linearly with
the level of restriction were identied as indicators of hunger. For
example, with increasing quantitative restriction, plasma levels of
an energy substrate, NEFA, decreased, presumably reecting
reduced adiposity, while glucose levels remained the same, leading
to an increased glucose/NEFA ratio. In a later study comparing three
alternative diets with quantitative restriction in growing broiler
breeders, glucose/NEFA sampled at the same time of day in each
treatment was lower under quantitative restriction (de Jong et al.
2005), seeming to suggest that these birds experienced less hunger
than those on the alternative diets. However, de Jong et al. (2005)
instead concluded that the lack of a 24 h prole makes it difcult to
compare quantitative restriction with alternative diets, presumably
because the higher postmeal glucose peak seen under quantitative
restriction may have affected the result (Tables 1 and 2). These two
studies illustrate the difculty with such measures, and in general
illustrate the difculty in validating measures with differing levels
of quantitative restriction and applying them to the quantitative
restriction versus alternative diets comparison.
Another issue with such studies is that peripheral indicators
that vary with the level of restriction may just measure the state of
nutrition, which may not necessarily correspond to the animals
negative emotional state (see below). Alternatively, it has been
argued that indicators that only begin to change after some
threshold level of restriction is reached may be more likely to
indicate hunger (Hocking et al. 1996).
A further difculty relates to how different measures should be
integrated. It is very common in animal welfare studies to use
a range of measures and interpret them together (e.g. using
 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288 279

behaviour to assist interpretation of physiology, Broom & Johnson
1993; Mason & Mendl 1993). However, research into effects of food
restriction often gives rise to different measures pointing to
different conclusions. For example, de Jong et al. (2005) found that
alternative diets (when compared to quantitative restriction) led to
reduced object pecking, more feeding and more sitting, suggesting
reduced hunger. However, the glucose/NEFA ratio was higher
(as already discussed), and the stress indicator heterophil/
lymphocyte (H/L) ratio was also higher. The authors explained the
H/L ratio nding in terms of increased stress and prolonged hunger
resulting from delayed satiety, because birds took much longer to
nish their food. In the light of these seemingly contradictory
results, they concluded overall that a low density diet might have
a small positive effect on broiler breeder welfare (de Jong et al.
2005, page 202).
In conclusion, the numerous physiological and behavioural
correlates of food restriction are not all necessarily measures of an
animals negative subjective state resulting from hunger. There are
particular difculties in extrapolating from quantitative restriction
to alternative diets. In general, there is a need for measures that are
specically designed to measure negative subjective states associ-
ated with hunger.
COMPARING LIKE WITH LIKE
Studies of differing levels of quantitative restriction result in
differences in energy intake and live weight change, and it seems
reasonable to assume that this will result in differences in the
animals perception of hunger/satiety. Experiments on alternative
diets typically involve comparison of one or more diets with
a control group fed a conventional quantitative restriction diet.
Where similar changes in empty body weight or live weight and
other indicators of energy reserves, such as backfat thickness in
sows, occur across treatment groups, fair comparisons of hunger
measures can be made to determine whether alternative diets can
reduce hunger (Table 3). Unfortunately, several studies of sows
using alternative diets designed to be isoenergetic with the quan-
titative restriction control ended up with treatment sows of
different weight (Table 3), either heavier than controls (e.g.
Ramonet et al. 1999, 2000c), or lighter and with less backfat (Matte
et al. 1994; van der Peet-Schwering et al. 2003a; Holt et al. 2006).
This may be because in previous studies it has been difcult to
predict the amount of energy sows will obtain through fermenta-
tion (Ramonet et al. 1999; Rijnen et al. 2001; De Leeuw et al. 2005a;
Jrgensen et al. 2007) or the extent to which bre will reduce the
absorption of other nutrients (Howarth et al. 2001) or, nally,
because comparisons were made on a live weight basis. Although
the best basis for designing isoenergetic diets is in terms of net
energy (Blaxter 1989), the studies reviewed here have all designed
diets to be isoenergetic in terms of metabolizable energy. Better
prediction of energy values should increase the accuracy of calcu-
lating isoenergetic diets in the future. An additional problem is that
changes in live weight may be inuenced by effects of diet quantity
and quality on gut ll (Day et al. 1996) and on gut wall proliferation
and this frequently makes it difcult to judge whether like is
compared with like. A comparison of empty body weight might be
more appropriate, correcting (at least) for differences in the weight
of gut contents, but this has never been reported in the studies
reviewed. A large number of other sow studies do not even report
the effect of diets on weight change or backfat (Table 3).
In studies of poultry, in particular where different diets are
offered ad libitum, growth rates and weights at the measuring
point(s) can also be very different between treatment groups
(Savory et al. 1996; Savory & Lariviere 2000). One option for dealing
with this is to adjust for weight in statistical analyses by tting it as
a covariate (Savory & Lariviere 2000). This is sensible, although it
does make the assumption that perceived hunger is linearly asso-
ciated with weight, which may not be valid (Hocking et al. 1996).
For the purposes of this review, we give greater weight to studies
where animal weights are similar across treatments (text in bold in
Tables 1 and 2; rst rows of Table 3), allowing fair comparisons to
be made of hunger measures at a given level of restriction. Other
studies may also be discussed to illustrate certain measures. With
this caveat, we can now proceed to a consideration of different
measures of hunger.
BEHAVIOURAL OBSERVATIONS AS INDICATORS OF HUNGER
Changes in observed behaviour in response to quantitative
restriction and alternative diets (reviewed in Lawrence et al. 1993;
Meunier-Salaun et al. 2001; Mench 2002; Hocking 2004; Ru & Bao
2004) are summarized in Tables 1 and 2 for broiler breeders and
sows, respectively, and discussed below. Following the design of
many studies in this area, the rst column of each table describes

Table 3
Comparing like with like? Different alternative diets and their effect on growth

Growth Ad libitum or rationed Broiler breeders Sows

Same Qualitative restriction (ad libitum) 18,19
Rationed alternative diet (basal plus) 3,5,26
Rationed alternative diet (isoenergetic) 11 11,17*

Different Qualitative restriction (ad libitum)

Rationed alternative diet (basal plus) 18,19
Rationed alternative diet (isoenergetic) 10 8,13,20,22,25y,26y,27y,29z

Different, but analysis includes weight as a covariate Qualitative restriction (ad libitum) 20,25
Rationed alternative diet (basal plus)
Rationed alternative diet (isoenergetic) 23

No information Qualitative restriction (ad libitum) 4,32

Rationed alternative diet (basal plus) 12,16
Rationed alternative diet (isoenergetic) 3,5,6,7,10,21,24x,30,31

Where alternative diets were rationed, this was done in one of two ways: basal plus means that all treatments were fed the same basic ration, but that additional ingredients
were added to this basal diet. Isoenergetic means that the total diet fed had the same calculated metabolizable energy (ME). Numbers for broiler breeders and sows refer to
references listed in Tables 1 and 2, respectively.
* Martin & Edwards (1994): differences in live weight gain between feeding treatments were not statistically signicant.
y
These three papers refer to the same core experiment, and Matte et al. (1994) reports treatment differences in growth between these sows.
z
van der Peet-Schwering et al. (2003b) gives no information about growth rate of sows on the different feeding treatments, but a companion paper, van der Peet-Schwering
et al. (2003a), does.
x
Rijnen et al. (2003) gives no information about growth rate of sows on the different feeding treatments, and neither does a companion paper, Rijnen et al. (2001), although
the companion paper states that energy obtained from nonstarch polysaccharides was greater than predicted, implying that there may have been differences.
280 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
how behaviour changes as quantitative restriction becomes more
severe, while the second (and in Table 1, third) column compares
behaviour of animals fed alternative diets to those under quanti-
tative restriction.
Typically under quantitative restriction, animals show signs of
arousal and anticipation in advance of food delivery, and then eat
their food rapidly. After feeding, various redirected oral behaviours
occur which are thought to reect a continuing unsatised feeding
motivation (Rushen 1984; Appleby & Lawrence 1987; Terlouw et al.
1991; Savory et al. 1992). Broiler breeders spot peck at the empty
feeder and drinker and at other objects such as oor, litter, walls
and cage bars, while sows sham-chew and nose, root or chew at the
trough, oor, chains and other xtures in the pen. If straw (or other
edible substrates) are available, sows will direct oral behaviours
towards these and eat them. The drinker is another target of
redirected oral behaviour, and both overdrinking and water spillage
have been reported in sows and broilers. The various forms of
redirected oral behaviours described can become stereotypic in
nature (unvarying and highly repetitive, Savory et al. 1992; Mason &
Latham 2004). Levels of stereotypy generally increase with
increasing quantitative food restriction (Savory et al. 1996; Brouns
et al. 1994a; Bergeron et al. 2000). Rushen (1984) suggested that
postfeeding stereotypies in the sow, including drinking, could be
analogous to the adjunctive behaviours (e.g. polydipsia) observed
between xed interval food rewards (Falk 1977).
Increased activity and foraging in response to food restriction
have been reported in a range of species including humans (Keys
et al. 1950; discussed in Garner 1997; Vitousek et al. 2004), labo-
ratory rodents (Dewasmes et al. 1989; Koubi et al. 1991; Hebebrand
et al. 2003), laboratory primates (Weed et al. 1997) and various wild
animals (Epling & Pierce 1988) and probably reect an adaptive
food-seeking response to food restriction. Correspondingly, levels
of other nonforaging-related behaviours such as preening in broiler
breeders were reduced under quantitative restriction. Wild animals
often reduce the performance of maintenance behaviours, play and
afliative behaviour when food is scarce (Loy 1970), presumably to
conserve energy or because there is reduced time for these as
foraging behaviour (food searching) predominates. Typically,
quantitative restriction results in an increase in behaviours relating
to foraging and in overall activity (indicated by reduced resting,
Savory & Lariviere 2000; Hocking 2004).
In contrast to behaviour during quantitative restriction, with
alternative diets animals eat more slowly, thus spending longer
eating. When food is ad libitum (qualitative restriction) the animal
shows a normal self-scheduled pattern of meals and intermeal
intervals (Zorrilla et al. 2005). With a few reported exceptions,
alternative diets result in a reduction in nonfood-directed oral
activities including stereotypic behaviour and excessive drinker
use, although time spent on total oral-related behaviours may be
the same (see below).
In summary, with a few exceptions, the behavioural effects of
the different feeding treatments discussed are largely agreed upon
by different researchers. There is little debate about whether
quantitative restriction results in hunger. We now consider the
different interpretations of the behavioural differences observed
when alternative diets are compared to quantitative restriction.
Normal versus Abnormal Behaviour
Alternative diets result in feeding and foraging behaviour that
appears normal in a number of ways. The self-scheduling of meals
under qualitative restriction, and the fact that meals end while food
is still available, could be argued (Meunier-Salaun et al. 2001) to
suggest an improvement in welfare because of the greater oppor-
tunities to express normal feeding behaviour. Naturalness of
behaviour is considered an important determinant of welfare by
some (Kiley-Worthington 1989; FAWC 1998: Freedom to express
normal behaviour), but not by others (e.g. Dawkins 1990; Broom &
Johnson 1993; Duncan 1993).
Loss of control is often seen as a key determinant of stress and
poor welfare. For example, rats, Rattus norvegicus, that were able to
predict and learn to use a lever to prevent or switch off mild electric
shocks showed considerably less stress (as indicated by the level of
gastric ulceration) than control animals receiving the same stimuli
but lacking control (Weiss 1972; Jensen & Toates 1997). It could be
argued that loss of control over the feeding schedule may have
similar negative consequences.
Under quantitative restriction, once food has run out, foraging
behaviour can be redirected towards other substrates and can
become stereotypic (references in Tables 1 and 2), while with
alternative diets, foraging behaviour is more often directed towards
food. Many argue that stereotypic behaviour is a sign of reduced
welfare, as it develops under suboptimal environmental conditions
(Dantzer 1986; Mason & Latham 2004) and often appears to reect
frustrated motivation (Mason et al. 2007). The heightened feeding
motivation implicit in food restriction has been identied as
a central factor in development of postfeeding oral stereotypies
(Dantzer 1986; Appleby & Lawrence 1987; Lawrence & Terlouw
1993; Mason & Latham 2004). The reduction in redirected oral
behaviours with alternative diets has thus been interpreted by
some as a sign of improved welfare (e.g. Bergeron et al. 2000;
Danielsen & Vestergaard 2001; Zonderland et al. 2004; Sandilands
et al. 2005). On the other hand, others (Savory et al. 1996; Dailey &
McGlone 1997; Savory & Lariviere 2000) noted that the total level of
foraging-related oral behaviours is often similar under quantitative
restriction and alternative diets (Tables 1 and 2). They suggested
that such oral behaviours are substitutable in terms of causation
and consequences and are thus functionally equivalent outlets for
unsatised feeding motivation (Savory & Maros 1993; Dailey &
McGlone 1997; McGlone & Fullwood 2001). Consequently, they
argued, when comparing quantitative restriction with alternative
diets that lead to similar weight gain, the occurrence of greater
redirected (and perhaps stereotypic) oral behaviours should not be
taken as a sign of poorer welfare if the duration of all oral behav-
iours combined remains the same overall. In a similar vein, the
reduction of stereotypies with alternative diets could simply result
from the greater time taken for eating and foraging behaviours,
rather than a proportional decrease in the level of stereotypy
(Meunier-Salaun et al. 2001; although some studies do show
proportional decreases, e.g. Bergeron et al. 2000). Lastly, stereo-
typic behaviour may aid coping in quantitatively restricted broiler
breeders since it can have dearousing consequences for those
performing it (Kostal et al. 1992; Savory et al. 1992, 1993a; Mason &
Latham 2004). The reduction in stereotypic oral behaviour with
alternative diets is thus not universally interpreted as a sign of
reduced hunger.
General Activity
A similar line of argument has been used in support of general
activity as a key measure of hunger. In two experiments (Savory
et al.1996; Savory & Lariviere 2000), broiler breeders were reared on
a range of feeding treatments differing in quality and quantity,
leading to a wide range of growth curves. In a comparison of
treatments, inactivity (sitting) was positively correlated with overall
weight gain, regardless of how weight restriction was achieved.
Based on this nding, it was concluded that quantitative and qual-
itative restriction did not differ in their consequences for hunger.
Reduced activity as a positive welfare indicator should of course not
be taken too far: inactivity in overweight birds fed ad libitum may be
because they are lame or are trying to avoid generating heat by
locomotion (Savory & Maros 1993; Nielsen et al. 2003).
 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
What is the Goal of Feeding Behaviour?
The assumption made by Savory et al. (1996) and Savory &
Lariviere (2000), that the level of chronic hunger is directly related
to growth rate, implies that if an animals growth is depressed
from some xed target (by any means) then chronic hunger will
result. A widely held position in livestock science is that an animal
of a given size and developmental stage has a relatively xed
target for growth or maintenance (often assumed to be a geneti-
cally determined maximum performance), which could be char-
acterized as maximization of energy intake subject to constraints
(Owen 1992; Kyriazakis 1994; Day et al. 1996, 1997; Weston 1996;
Emmans 1997). In this view, qualitative restriction prevents
animals from achieving their desired target, in most cases because
of a constraint on food processing by the gastrointestinal tract, for
example because of the greater volume or slower digestion of
such diets (Day et al. 1996; Emmans 1997; Tsaras et al. 1998;
Whittemore et al. 2002). These animals are sometimes said to be
experiencing metabolic hunger (Day et al. 1996; Savory et al.
1996). Similar concerns have been expressed about high-yielding
dairy cows fed exclusively on grass and other forages (Webster
1995, 2005).
An alternative view of what determines food intake is that,
instead of xed targets, animals have more exible goals for food
intake and growth, depending on a balance of benets and costs
(reviewed in Illius et al. 2002). In this view, the balance of benets
and costs might vary with the available food quality, resulting in the
animal modifying its goal when alternative diets are provided.
Food is benecial, providing energy and other nutrients essential
for maintenance, growth and reproduction, but also carries
extrinsic and intrinsic costs. Extrinsic costs include exposure to
predation and other environmental costs during foraging, and the
opportunity cost of spending time foraging which could be usefully
spent on other activities (these were present in the wild ancestors
of captive animals, so may inuence evolved behavioural mecha-
nisms). Intrinsic costs include (1) the cost of tissue damage from
oxidative metabolism resulting in reduced life span (Tolkamp &
Ketelaars 1992), (2) exposure to toxins and parasitic organisms
(Hutchings et al. 2000, 2003) and (3) increased dental wear
resulting in reduced foraging life span (Owen-Smith 1994). In
support of this view are various observations that do not seem
compatible with the idea of xed constraints, for example the
capacity of animals to increase intake of the same food when
energy demands are high (e.g. during lactation or cold weather,
Ketelaars & Tolkamp 1992, 1996; Illius et al. 2002). Indeed, the size
or function of some part of the gastrointestinal tract (e.g. stomach
size) might appear to be a constraint in an individual animal under
certain conditions, but in most cases this is not an absolute
constraint and could change under natural selection if this
increased Darwinian tness (Barboza & Hume 2006). The conse-
quences of this view for animal welfare would be that hunger is
only relative to the specic/current nutritional environment, as
long as available food qualities are within the normal range for the
species. Since animals are able to optimize intake on any food
quality, hunger only occurs when animals cannot choose their own
level of intake, when food is not freely available, as under quanti-
tative restriction (Lawrence et al. 2004).
With one exception (Lawrence et al. 2004) the optimization
approach has not been discussed in relation to the controversy
surrounding alternative diets. However, a number of authors who
have argued for animal welfare benets of alternative diets appear
to question the maximization of energy intake subject to
constraints position outlined above, discussing other factors which
they believe to inuence hunger or satiety (reviewed in Howarth
et al. 2001). For example, alternative diets may increase the ll of
the gastrointestinal tract (Robert et al. 1993; Day et al. 1996;
281
Whittaker et al. 1998, 1999; Meunier-Salaun et al. 2001; De Leeuw
et al. 2004; de Jong et al. 2005) and, depending on the bre source,
lead to a decrease (Johansen et al. 1996) or an increase (Roberfroid
1993) in gastric emptying times. In sows, certain brous ingredi-
ents can be fermented in the hindgut (De Leeuw et al. 2005a)
releasing volatile fatty acids (Mroz et al. 1986) that may promote
satiety (Rerat 1996; Whittaker et al. 1998; De Leeuw et al. 2004,
2005a). Alternative diets may result in more gradual energy release
postmeal resulting in more uniform levels of metabolic substrates
(e.g. glucose, acetate) and hormones (e.g. insulin) in blood plasma
(Brouns et al. 1994b; Rushen et al. 1999; De Leeuw et al. 2004,
2005b). Campeld & Smith (2003) argued that meal initiation may
result from a drop in plasma glucose, supporting the idea that
uniform levels may promote satiety. These authors and others
(Howarth et al. 2001; Levitsky 2005; Rolls et al. 2005a) appear to be
assuming that the animal integrates many different signals that
determine how severe the experience of hunger is. In this view,
energy consumed and stored in the body is important, but is only
one component of these signals.
These many different signals views, as well as the optimiza-
tion idea above, would also support the prospect that changing
from quantitative restriction to alternative diets could improve
animal welfare by reducing hunger. For example, discussing this
evidence along with the behavioural effects of qualitative restric-
tion (reduced stereotypy and activity) led Zonderland et al. (2004,
page 19) to conclude that for sows This all indicates that.a diet
containing a high amount of sugar beet pulp can improve satiety.
The physiological literature also provides some support for the idea
that many signals are involved in the control of food intake
(reviewed in Blundell 1991; Stanley et al. 2005; Strader & Woods
2005; Wynne et al. 2005 for mammals; Savory 1999; Boswell 2005
for birds). However, the way in which all of these signals interact
and are weighted, resulting in sensations of hunger, feeding
motivation and resulting behaviour, remains unclear. In some
sections of this literature, there is a strong emphasis on the primacy
of physiological mechanisms to restore energy balance in the
longer term, in particular, mechanisms to restore body weight
following deprivation (Schwartz et al. 2000; Wynne et al. 2005),
while others allow for the possibility that there is no set point of
weight that is tightly regulated; instead, weight can depend on
a number of other factors including food quality (Mela & Rogers
1998; Howarth et al. 2001; Levitsky 2005; Rolls et al. 2005a;
Tolkamp et al. 2007).
In summary, there is broad agreement between studies about
behavioural changes seen when food quantity is restricted, and on
the changes in behaviour when qualitative restriction is used
instead. These behavioural changes are interpreted by some
authors as signs of improved animal welfare, but others dispute this
interpretation. These disputes appear to arise from different
implicit assumptions about (1) denitions of welfare (e.g. the
importance of normal versus abnormal behaviour), (2) the inter-
pretation of welfare measures, and (3) what determines an animals
food intake goal, as well as some issues concerning study design
which may be overlooked.
BEHAVIOURAL TESTS OF FEEDING MOTIVATION
TO MEASURE HUNGER
Tests of feeding motivation are a valuable tool in the assessment
of hunger (Day et al. 1997), because, more than any other measure,
we expect feeding motivation to reect directly the animals own
subjective state of hunger (Dawkins 1990). Feeding motivation has
been measured using (1) feeding rate when a limited amount of
food or feeding time is offered, (2) compensatory feeding, where
the ad libitum intake over a number of days is measured following
a period of restriction, and (3) operant conditioning procedures,
282 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
where extra food can be obtained by pecking a key or pressing
a panel or lever. All of these measures increase as the amount of
food available is reduced (quantitative restriction, rst column in
Tables 1 and 2), but as with other measures, the picture becomes
more complex when one compares quantitative restriction with
alternative diets. With two exceptions (Sandilands et al. 2005,
2006), these tests have not been applied where animals on
different diets had similar growth rates, which makes drawing
conclusions for our purposes difcult (Tables 13).
Feeding Rate
Feeding rate usually increases with increasing food deprivation.
Feeding rate and time spent eating have a number of difculties as
measures of hunger where food quality varies, because feeding rate
usually declines when lower quality food is offered (Zuidhof et al.
1995; Ramonet et al. 1999, 2000c). In addition, alternative feeds
based on bulky ingredients may lead to consumption of water within
a feeding event (Kyriazakis et al. 1994) leading to a reduction in the
feeding rate. Learning may also be a factor; animals fed a restricted
quantity of food are used to eating quickly, both because high-quality
food is eaten more quickly than low-quality food (Johnson & Collier
1987) and because food-restricted animals may experience intense
food competition (Nielsen 1999). As a result of these factors animals
may be more likely to speed up feeding rate in a test. Also, because
animals on quantitative restriction often nish their daily ration in
a shorter space of time than animals on qualitative restriction, they
may eat more because, depending on when testing takes place, it is
generally longer since they last fed. To compare animals on alterna-
tive diets raises the question of how long they should be deprived of
food before testing. There is overall a risk that treatment comparisons
become arbitrary as a result of decisions made to overcome these
difculties (Sandilands et al. 2005).
Compensatory Feeding Tests
Where previously restricted animals are allowed ad libitum
access to food, their total intake during this compensatory feeding
period can be used as a measure of the hunger that has resulted
from the restriction period. Since a period of restriction will result
in smaller, lighter animals, there needs to be some adjustment of
expected intake accounting for body weight. This then raises the
problem of what is the correct scaling method to use for this
adjustment. For example, de Jong et al. (2003) used metabolic size
(body weight3/4). However, when we analysed their data on ad
libitum-fed growing birds, we found that food intake per unit of
metabolic size decreased as birds grew, from 0.5 to around 0.4 g/
body weight3/4, suggesting that a xed scaling method is not
appropriate, which makes a fair comparison difcult.
There are additional difculties when considering alternative
diets. In particular, the question of which food to offer during
testing is problematic. Animals fed a qualitative restriction diet are
already at ad libitum intake on this food, so by denition would not
increase their intake if tested with the same food. Thus this tech-
nique reveals the discrepancy between rationed and ad libitum
intakes, and implicitly assumes that ad libitum-fed animals are not
hungry. As discussed above, a number of researchers would dispute
the idea that ad libitum feeding on poor-quality food does not result
in hunger (e.g. Owen 1992). To compare compensatory intake in
units of energy (de Jong et al. 2005) is not a solution since ad
libitum energy intake differs with food quality (Savory et al. 1996;
Whittemore et al. 2002; Tolkamp et al. 2005; Johnston et al. 2006).
Using a uniform food during compensatory feeding tests would
also be problematic because of the scaling issue discussed above
and also because animals will have adapted to a particular food
type (Nielsen 2004). This is discussed further below.
Operant Responding for Food
Operant conditioning for a food reward is an effective way of
measuring feeding motivation, since the ratio of cost (e.g. lever
pressing) to reward (food) can be altered by the experimenter. The
method has been validated for quantitative restriction: increasing
restriction results in increasing feeding motivation (rst column in
Tables 1 and 2). However, when comparing quantitative restriction
to alternative feeding systems, because animals are accustomed to
different foods, it is not obvious which food they should be offered
during the test. This is also a problem for the tests of feeding rate
and compensatory feeding already discussed.
When the usual (treatment) food is provided as a reward
(Robert et al. 1997; Savory & Lariviere 2000), the animal receives its
familiar food, but it is then difcult to decide what constitutes
equivalent responding when comparing treatments. Offering an
equivalent weight of food (Robert et al. 1997) to each treatment
means that different levels of energy are obtained per lever press.
This is a problem, because more energy-dense foods (and greater
energy intakes) are more attractive: rats will perform an operant
task at higher ratios for the same weight of a higher quality (more
energy-dense) food (Johnson & Collier 1987). In another study,
instead of equal weight of reward food, a standard time of access
(e.g. 3 s, Savory & Lariviere 2000) was offered. Because of the issue
of different feeding rates discussed above, this may be a worse
solution, since animals used to qualitative restriction may eat less of
their lower quality food reward during each 3 s reward.
When all treatments are tested with the same food (Lawrence
et al. 1989; Ramonet et al. 2000a), it is possible to compare directly
the number of rewards obtained across treatments. However, the
reward food is often of high quality. For animals fed on alternative
diets, the food reward represents a greater contrast with their usual
food than for animals on quantitative restriction. This contrast may
result in a greater feeding motivation, and thus greater responding
in these animals (Ramonet et al. 2000a; Savory & Lariviere 2000).
These differences in reward type can explain the ndings of
different studies using sows. Where the treatment (usual) food was
used as a reward, sows fed on alternative diets and offered the same
food in an operant regime showed less responding than conven-
tionally restricted sows (Robert et al. 1997) even though they were
gaining less weight on this diet (Matte et al. 1994). This result could
mean that alternative diets reduce hunger and feeding motivation,
or, alternatively, that the lower energy available in 10 g of the
alternative diet made it less attractive and less motivating in the
test. In studies where a standard diet was used as a reward, no
differences in operant responding were found between sows fed on
alternative diets and quantitative restriction (body weight changes
not reported, Lawrence et al. 1989; Ramonet et al. 2000a). This
could mean that these sows were equally hungry, but, alternatively,
sows on the alternative diets might have been less hungry, but
worked harder in response to the greater contrast in perceived food
quality (Ramonet et al. 2000a).
Operant tests are often repeated at different times of day, and
these results can be revealing, when comparing how treatments
differ (Day et al. 1996; Robert et al. 1997; Savory & Lariviere 2000).
This approach is not affected by the problems over the nature of the
reward discussed above, because no direct quantitative comparison
is made between treatments. Typically with alternative diets,
operant responding for food after a meal is low (Robert et al. 1997),
and stays low for longer (Day et al. 1996) before beginning to rise
and is high again before the next meal. In contrast, under quanti-
tative restriction, operant responding for food is similarly high at
different tested time points (Lawrence et al. 1988; Ramonet et al.
2000a). For example, Savory & Lariviere (2000) fed broiler breeders
at 0900 hours and tested operant responding for food at 1000, 1300
and 1600 hours. Qualitative restriction treatments had lower
 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
feeding motivation in the 1000 hour test than the later tests, while
the quantitative restriction treatments had similar motivation in all
tests. This is usually interpreted as indicating that alternative diets
result in satiety for at least part of the day (Robert et al. 1997; Savory
& Lariviere 2000), although others have interpreted this result
more in terms of a constraint, where for example gut distension
inhibits further feeding, despite a continuing demand for energy
(metabolic hunger, Day et al. 1996). Once again, the different
theories as to what determines an animals food intake goal can
result in differing interpretations of the same data.
CHOICE TESTS TO COMPARE FEEDING SYSTEMS
Animals are expected to prefer situations that they perceive as
enhancing their welfare (Hughes & Black 1973; Dawkins 1976,
1990; Kirkden & Pajor 2006). When animals are offered a choice
between different foods ad libitum, they usually prefer high-quality
(energy-dense) food (Mela & Rogers 1998; Guillemet et al. 2007),
although not exclusively (Keunen et al. 2002). However, in
a comparison of quantitative restriction and alternative diets, the
different foods are not available ad libitum which raises the ques-
tion of whether animals still prefer a high-quality reward when
there is very much less of it. Taylor (1977) trained mildly food-
deprived (8090% of ad libitum weight) rats to run for either four
low-quality pellets (1.0 kcal/g, equivalent to 4.2 kJ/g) or one high-
quality one (4.0 kcal/g, equivalent to 16.7 kJ/g). After 12 days of ve
daily trials, the contingencies were swapped. Rats shifted from one
high-quality pellet to four low-quality ones ran more quickly, while
those shifted from four low-quality pellets to one high-quality
pellet slowed down. This contrast effect suggests that the four low-
quality pellets were perceived as more attractive. This experiment
was not ideal, since it was not performed under a closed economy
(additional food was available outside the apparatus) and no direct
choice was offered. Comparing the feeding choices of animals
between large quantities of low-quality food and smaller quantities
of high-quality food in a closed economy could give valuable insight
into the relative value that animals place on food quality and
quantity. To the best of our knowledge, this seemingly simple
experiment has not been tried before in any species, and would be
relevant to the questions posed in this paper. This idea could be
developed by manipulating different nutritional components and
offering choices between meals or feeding systems. In this way, the
relative importance of energy and other nutrients, gut ll, feeding
time, etc. to the animal could be assessed.
Another similar approach might be to train animals to associate
a particular location with the experience of a particular feeding
system. When an animal was returned to this location, measures of
frustration or aversion (such as the motivation to leave, or to move
to a location associated with a different feeding system) could be
used as an integrated measure of their overall welfare experience
of that system.
PHYSIOLOGICAL MEASURES OF HUNGER
Feeding Physiology
The physiological and neural control of feeding is a subject of
extensive research, particularly in mammals (Blundell 1991; Saper
et al. 2002; Stanley et al. 2005; Strader & Woods 2005; Wynne et al.
2005) but also in birds (Savory 1999; Boswell 2005). There are
a growing number of hormones, metabolites and neuropeptides
known to be involved in the control of feeding. Central control
involves an interaction between regions within the hypothalamus
and brainstem and reward centres (Stanley et al. 2005; Strader &
Woods 2005; Wynne et al. 2005). In mammals there are mechano-
receptors in the stomach responsive to volumetric cues (de Graaf et al.
283
2004) and chemoreceptors in the intestine that respond to the
presence of nutrients (e.g. cholecystokinin; ghrelin, glucagon-like
peptide 1, Powley & Phillips 2004; Strader & Woods 2005). Many of
these signals are integrated in the brainstem in the nucleus tractus
solaris (Schwartz et al. 2000). In birds and mammals, nervous and
endocrine signals are sent from energy stores in the liver (Friedman
et al. 2005) and adipose tissue (e.g. leptin, insulin, de Graaf et al. 2004)
to the arcuate nucleus of the hypothalamus which controls energy
balance (e.g. neuropeptide Y, agouti-related protein, Boswell 2005).
Some attempts have been made to link these physiological processes
to the self-reported subjective perception of hunger, palatability or
satiety in humans (Howarth et al. 2001; Yeomans et al. 2004; Fin-
layson et al. 2007), but the picture remains complex. The main dif-
culty is that it is largely unclear how all the different processes are
weighted and integrated, and, most importantly for our purposes
here, how they relate to an animals subjective experience of hunger.
Some aspects of feeding physiology have been used in broiler
breeders and sows on different feeding treatments, either to
measure hunger or to understand better the physiological
processes underlying behavioural changes (Tables 1 and 2). These
include measures of energy substrates such as glucose and NEFA,
and the hormones that regulate them, such as insulin and glucagon.
These measures typically undergo changes over the day in
relation to meal patterns, making point sampling (de Jong et al.
2003, 2005) difcult to interpret, particularly when comparing
quantitative restriction with alternative diets which often result in
different meal durations and patterns (Rushen et al. 1999). The
dynamic processes of energy balance also create difculties of
interpretation. Energy substrates may be in the blood because of
absorption during a meal, or indicate the presence of, or utilization
of, body energy stores. For example, plasma NEFA is higher in
animals with high lipid reserves (Chen et al. 2006) but also rises
during fasting (Van der Wal et al. 1999; Toscano et al. 2007).
Because of the link with adiposity, de Jong et al. (2003) considered
a high glucose/NEFA ratio as a possible measure of hunger in broiler
breeders. The difculties with this measure have already been
discussed in an earlier section.
Stress Physiology
Measures of stress physiology such as glucocorticoids (e.g.
cortisol and corticosterone; CORT) and other measures of HPA
functioning are widely used as a measure of animal welfare
(reviewed in Mormede et al. 2007). Their popularity stems from
their generality, being released in response to a range of aversive,
unpleasant situations, especially in the light of ndings showing
that the psychological component of the stressor is the main
determinant of the magnitude of response (Mason et al. 1968;
Mason 1971; Weiss 1971; Veissier & Boissy 2007).
There are a number of problems with the use of CORT as
a measure of hunger.
(1) CORT rises in response to pleasurable or exciting stimuli,
reecting emotional arousal (Mason & Mendl 1993), so a higher
cortisol peak just before feeding in quantitatively restricted sows
than in sows on alternative diets may reect increased excitement
in anticipation of the small high-quality daily meal (Ramonet et al.
2000b). A similar observation can be made concerning heart rate
rises in these situations (Robert et al. 1997).
(2) CORT is not usually a good measure of a chronic stress (such
as that which might result from chronic food restriction), since the
HPA axis adapts and CORT levels tend to return to baseline. Chal-
lenging the HPA axis to reveal changes in responsiveness are often
used (e.g. corticotropin-releasing hormone, CRH, challenge, Jarvis
et al. 2006) to overcome this problem. A challenge test using adre-
nocorticotropic hormone (Spoolder et al. 1996) showed no differ-
ences in cortisol response of sows on different feeding treatments.
284 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
(3) CORT has various metabolic effects, all of which result in an
increase in or maintenance of glucose levels in the blood (Tempel &
Leibowitz 1994). These include mobilization of amino acids from
muscle and lypolysis in adipose tissue, providing substrates for
gluconeogenesis in the liver. CORT also interacts with brain
substrates important in the control of food intake. CORT in the
blood plasma shows a diurnal rhythm which is affected by meals
(Mormede et al. 2007), reecting its metabolic role and making it
difcult to compare treatments with different meal patterns, such
as quantitative restriction and alternative diets. In general, the
important metabolic role of CORT makes it particularly difcult to
interpret it as a welfare measure to determine levels of hunger in
different feeding treatments.
(4) In studies of broiler breeders, CORT declines with weight, in
ad libitum-fed as well as in quantitatively or qualitatively restricted
birds (Savory et al. 1996; de Jong et al. 2002; Sandilands et al. 2005).
This confound has not been taken into account when interpreting
CORT differences observed at a given age between treatments that
result in different body weights.
In practice, CORT levels are higher in severely food-restricted
broiler breeders than in more generously fed birds of the same age,
but quantitative restriction and alternative diets show no differ-
ence (Table 1). We could nd no papers comparing CORT levels of
sows at different levels of quantitative restriction. CORT levels are
similar in sows on quantitative restriction and alternative diets, but
have a higher peak postmeal in the former, suggesting a metabolic
role for this hormone (Table 2). The lack of differences in CORT
between treatments combined with the difculties highlighted
above mean that this measure is not a useful way of detecting
differences in hunger between feeding treatments.
In poultry, measures or ratios of white blood cells are a common
method of animal welfare assessment, in part because they are
inuenced by, and thus an indicator of, chronically elevated corti-
costerone (Maxwell 1993). In an important study to validate stress
measures in poultry (Gross & Siegel 1983), plasma CORT levels were
highly variable in response to chronic social stress or chronic
addition of CORT to the feed. Blood heterophil levels rose and
lymphocytes fell in a much more consistent way in response to
these treatments, suggesting that the HLR was a useful integrating
measure of stress. If correct, this means that HLR is less likely to
suffer from one of the problems outlined for CORT: changes taking
place over the day, and in response to meals. However, the rationale
behind the use of HLR (i.e. its association with CORT and the HPA
axis) means that, in principle, many of the other criticisms still
apply. It is then perhaps not surprising that, in practice, when HLR is
applied to the problem of hunger, the results are confusing:
different studies nd that HLR either rises, stays the same or falls in
response to different levels of quantitative restriction and when
comparing these with alternative diets (Tables 1 and 2). A similar
confused picture emerges in both poultry and pigs when other
immune markers have been used in comparisons of alternative
diets to quantitative restriction (Tables 1 and 2).
A variety of enzymes associated with tissue damage during
various forms of stress (e.g. creatine kinase (CK; muscle), lactate
dehydrogenase (heart muscle), aspartate transaminase (liver),
alkaline phosphatase (turnover of bone tissue)) have been applied
to broiler breeders on different diets by Hocking and coworkers
(Table 1), although it is difcult to see why stress in these tissues
should be expected under food restriction. These markers are likely
to have different meanings in this case. For example, raised CK was
found in transported broilers suffering from heat stress (Mitchell
et al. 1992), but was reduced under quantitative restriction, prob-
ably because CK increases with growth rate (Table 1).
In summary, feeding physiology measures have generally been
underused in this eld of research, although in general it is difcult
to relate peripheral measures to the animals subjective experience
of hunger. The metabolic function of CORT also makes stress-based
measures problematic for use as measures of hunger. There is
poorer agreement between different studies when physiological
indicators of hunger are considered compared to behavioural
indicators (Tables 1 and 2).
WIDER IMPLICATIONS
Many of the issues considered in this review are of more general
interest to other elds of research. Researchers interested in obesity
in humans (and companion animals) pose similar questions to
those addressed in this review. Can low-quality foods (typically
those containing low energy but high bre) increase satiety,
assisting the overall reduction in energy intake required for weight
loss? Or do low-quality foods leave a person full but unsatised
(metabolically hungry?) and likely to compensate by increasing
intake of other foods? Similar to the debate over qualitative and
quantitative restriction in animals these questions are controversial
in obesity research. Some authors believe that such high-bre or
low energy density diets can be effective in the long term (Duncan
et al. 1983; Poppitt & Prentice 1996; Doucet & Tremblay 1997;
Howarth et al. 2001; Yao & Roberts 2001; Astrup et al. 2002; Lev-
itsky 2005; Rolls et al. 2005a, b), while others suggest that the
benets are short-lived and that homeostatic mechanisms act to
restore the level of energy intake (Roehrig 1991; Drewnowski et al.
2004; Stubbs & Whybrow 2004). The further research topics that
we propose would also be instructive to researchers interested in
obesity. (1) How are different physiological satiety signals inte-
grated and weighted leading to feeding decisions, and how do these
signals respond to manipulations of food quality? (2) What do
animals (or people) choose when asked to trade off food quality and
quantity in a long-term food preference study?
The question of what animals are trying to achieve when they
eat has been addressed in the behavioural ecology optimal
foraging literature (reviewed in Stephens & Krebs 1986; Bateson
2003). However, the issue of how animals make decisions about
food quantity versus quality has not been directly addressed.
Certain related questions about trade-offs have been considered,
for example studying how animal choices change in response to
depleting patches, or to increasing travel costs between food
patches in terms of time and energetic costs (Kacelnik 1984; Todd &
Kacelnik 1993; Bautista et al. 2001). The extent to which animal
decision making in practice conforms to theoretical predictions
based on maximizing energy intake rate has been a focus of interest
(Tolkamp et al. 2002). For example, animals prefer immediate small
rewards to larger rewards that are delayed or unpredictable
(Abeyesinghe et al. 2005; Kalenscher et al. 2006; van den Bos & de
Ridder 2006; Shapiro et al. 2008), even when the latter choice
might result in more food and a greater rate of energy intake. It
would be interesting to investigate how animals respond to a large
meal that takes longer to consume and whether this is treated in
the same way as a delay. The time taken to complete the meal is
analogous to a delay, but, on the other hand, the food is available
immediately, rather than existing only as an uncertain (and inexact)
expectation. Impulsive choices for immediate reward may mean
that animals would prefer small quantities of high-quality food in
a choice test because they offer immediate gratication, even
though a larger quantity of lower quality food might be more
satiating over a longer period. On the other hand, the phenomenon
of contrafreeloading suggests that animals given free food will
often also work for food in operant or naturalistic tasks, rather than
maximizing their rate of energy intake by consuming only the free
food (Osborne 1977; Forkman 1996; Inglis et al. 1997; Bean et al.
1999; Lindqvist et al. 2006). It could be that animals are motivated
to perform their natural foraging behaviour (behavioural satiety
Kacelnik 1987; Gardner & Gardner 1988; De Leeuw 2004)
 R.B. DEath et al. / Animal Behaviour 77 (2009) 275288
suggesting that qualitative restriction might be preferred. Alter-
natively, contrafreeloading may occur because animals sample
from different options to gain information about the environment
(Inglis & Shepherd 1994; Forkman 1996; Bean et al. 1999). In this
case, some visits to both options would be expected in an experi-
ment offering animals a choice between quantitative restriction
and an alternative diet. However, the relevance of this discussion of
contrafreeloading may be lessened by the observation that it is
considerably reduced when animals are hungry (Inglis & Ferguson
1986; Bean et al. 1999; Talling et al. 2002).
CONCLUSIONS
Although there is little doubt that animals undergoing quanti-
tative food restriction are hungry by our denition, the question of
whether alternative diets lead to reduced hunger remains contro-
versial. Assessing any aspect of animal welfare involves the use of
indirect indicators to reveal something about the animals under-
lying subjective state. Even when research ndings are agreed
upon, the meaning of these for hunger can be interpreted differ-
ently. This is because, either explicitly or implicitly, researchers are
making different assumptions about the ultimate goal of food
intake, and thus whether energy intake targets are xed or
dependent on the available food quality. Critical tests for dis-
tinguishing between these hypotheses need to be devised. Greater
use of diets of varying quality in fundamental feeding physiology
research and experiments designed to test animals preferences
between different feeding systems would offer major opportunities
for progress in this area.
Acknowledgments
We had useful conversations with Melissa Bateson, Gerry
Emmans, Vicky Sandilands, Marian Dawkins, Claire Williams, Pat-
ricia Riddell, Louise Scott, Louise Buckley and Susan Jarvis about
some of the issues raised here. The SAC is supported by the Rural
and Environment Research and Analysis Directorate of the Scottish
Government.
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