CAB Reviews 2016 11, No.

010

Animal-based indicators to assess welfare in zoo animals

X Manteca*, M Amat, M Salas and D Temple

Address: School of Veterinary Science, Universitat Autònoma de Barcelona, 08193 Bellaterra (Barcelona), Spain

*Correspondence: X Manteca. Email: xavier.manteca@uab.es

Received: 24 February 2016

Accepted: 11 May 2016

doi: 10.1079/PAVSNNR201611010

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

© CAB International 2016 (Online ISSN 1749-8848)

Abstract

Animal welfare is a priority for modern zoos and science-based welfare indicators are needed.
Welfare indicators can be divided into environment-based and animal-based indicators.
Environment-based indicators are usually easier to measure, but only animal-based indicators
provide direct information on the welfare of animals and are therefore preferred. Animal-based
indicators include abnormal behaviours; changes in the frequency, duration or intensity of normal
behaviours; disease prevalence or incidence; life span; body condition, physiological parameters;
telomere length; and keeper ratings. Some of the abnormal behaviours most commonly used to
assess welfare are stereotypies, apathy, regurgitation-reingestion and feather-damaging behaviour.
Changes in sleep, feed intake, rumination, displacement behaviours, anticipatory behaviour, play,
affiliative behaviour, aggression and maternal behaviour can also be used to assess welfare in zoo
animals. There is no single indicator that can provide all the information needed to assess the welfare
of an animal or group of animals. Further, all potential welfare indicators have shortcomings and
methodological limitations. Therefore, several indicators have to be used to assess zoo animal
welfare and they should be checked for validity, reliability and feasibility. Also, both positive and
negative indicators of welfare should be used. One area deserving further research is the
development of welfare assessment protocols that combine the best indicators for a given species or
taxonomic group. Some of the protocols developed for farm animals could be applied to zoo animals.
Most research on welfare assessment of zoo animals refers to mammals and birds and identification
of welfare indicators for reptiles, fish and amphibians is another research priority.

Keywords: Animal welfare, Zoo, Behaviour, Stress

Review Methodology: Scientific papers have been searched in CAB Abstracts and PubMed using the following keyword search terms:
‘zoo AND animal welfare’ and ‘stress AND animal welfare’. Also, all issues of the journals Animal Welfare, Applied Animal Behaviour
Science and Zoo Biology published after 2005 have been systematically searched for papers on zoo animal welfare, and those including
information on animal-based indicators that could be used in zoo animals were selected. The references in the articles found have also
been used to check for additional relevant material. The authors also spoke to their colleagues to check for upcoming research.

Introduction animals in captivity [2, 3], which has been identified as a

Animal welfare has become a priority for modern zoos. For
example, in 2015 the World Association of Zoos and
Aquariums launched its animal welfare strategy Caring for
Wildlife, urging zoos to provide the best possible standards
of animal welfare [1]. Scientifically-validated animal welfare
indicators are therefore needed to identify problem areas
and monitor progress when improvement strategies are
implemented. As a result, there has been a growing interest
in the development of welfare assessment tools for wild
research priority for the zoo community [4].
Animal welfare assessment should be based on the fact
that animal welfare includes the physical and mental health
of animals, as well as their behaviour [5–7]. As a result of
the multi-dimensional nature of animal welfare, there is no
single indicator that can provide enough information to
assess the welfare status of an animal or group of animals;
consequently, several indicators have to be used when
assessing welfare [8–10]. Animal welfare indicators can be
divided into two broad categories: environment-based and

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2 CAB Reviews
animal-based indicators. Many environment-based indi-
cators have the advantage of being easier to measure than
animal-based indicators. However, a given environmental
feature may have a variable and often an unpredictable
effect on the welfare of animals, as its effect will depend on
the temperament of each individual animal and on its
interaction with other environmental features. This is why
animal-based indicators, which provide direct information
on the welfare of animals, are generally preferred
[3, 10–12]. Ideally, animal welfare indicators should be
checked for validity, reliability (both intra- and inter-
observer reliability) and feasibility before being used [10].
Although most research on animal welfare has focused on
negative indicators of welfare, positive indicators are
equally important.
The objectives of this paper are to describe the main
animal-based indicators that can be used in zoo animals
and to discuss their rationale as well as their conceptual
and methodological limitations. The following categories
of animal-based indicators will be covered in this review:
abnormal behaviours; changes in the frequency, duration
or intensity of normal behaviours; disease prevalence
and incidence; life span; body condition; physiological
parameters; telomere length; and keeper ratings.
Abnormal behaviours are defined as behaviours that are
never or very rarely seen in the wild and that are a
consequence of poor welfare [13].
Abnormal behaviours
Stereotypies
Stereotypies were originally defined as repetitive, invariant
behaviours that have no obvious function [14]. Stereotypies
have also been defined as repetitive behaviours induced by
frustration, repeated attempts to cope and/or central
nervous system dysfunction [15]. This second definition
acknowledges the fact that stereotypies are not always as
invariant as originally thought and that some stereotypies
may help animals cope in inadequate environments [16, 17].
Some of the most common stereotypies in zoo animals
include pacing, repeatedly licking or biting objects, and
repetitive movements of different body parts while the
animal is stationary. The frequency of each type of
stereotypy varies according to the taxonomic group; for
example, pacing seems to be most common in carnivores,
while oral stereotypies (including, e.g. biting or licking
objects) are particularly common in ungulates [18]. Even
within a given taxonomic group, species may differ not only
in the extent to what they develop stereotypies [19, 20],
but also in the form of stereotypy they display. For example,
the most common stereotypy in pinnipeds is repetitive
swimming, but walruses develop a stereotypy in which they
rub their tusks against the walls or floor of the pool.
Walruses appear to be the only pinniped species that
display oral stereotypies and this has been linked to their
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normal foraging behaviour [21]. Stereotypies have been
described in mammals and birds [22], and whilst it is
uncertain whether they occur in other taxonomic groups,
some repetitive behaviours in fish might be equivalent to
stereotypies [23, 24]. Stereotypies are frequent in several
species of zoo animals and in some cases account for a
significant proportion of the time budget of the animal. For
example, a very high percentage of zoo elephants [25] and
giraffes [26] show stereotypies.
Different types of stereotypies may have different causes.
For example, oral stereotypies in herbivores appear to be
caused, at least partly, by their inability to perform normal
foraging behaviour and rumination when kept in captivity
[27, 28]. In carnivores, pacing results from a combination of
several factors, including lack of space and the inability to
perform normal behaviour. It has been shown that species
of carnivores that travel long distances in the wild are more
likely to show stereotypies when kept in captivity [19, 20].
Stereotypies may also result from medical conditions [29].
Stereotypies are one of the most used indicators of poor
welfare and there is no doubt that they are indeed very
useful, as their main causes are linked to frustration or
behavioural deprivation [15]. Moreover, stereotypies may
contribute to the development of medical problems,
including dental and foot conditions [30, 31]. However,
using stereotypies as welfare indicators is not without
problems [16, 32]. First, stereotypies are not always easy to
identify; for example, the most common stereotypy in
marine mammals is repetitive swimming in a fixed pattern
around the pool, but this could also be functional patrolling
behaviour [33]. Also, if a given stereotypy has been shown
for a long period of time, it may become ‘fixed’ and
therefore the possibility exists that an animal currently kept
in a suitable environment displays stereotypic behaviour as
a result of it having been kept in an inadequate environment
in the past [32]. Stereotypies may appear as a result of
learning, in which case they are not necessarily good
indicators of poor welfare. Finally, many studies on
stereotypies in zoo animals do not include the time when
animals are kept in indoor facilities at night and their results
may be misleading, as stereotypies may be more frequent
when animals are indoors [34].
Apathy
Apathy, defined as a reduction in goal-oriented behaviour,
is a common feature of several psychiatric disorders of
humans, including depression [35]. In animals, apathy has
been defined as abnormal inactivity and lack of interest in
environmental stimuli [36]. Specific signs of apathy in
animals include altered self-grooming, reduced interaction
with conspecifics, impaired maternal care and decreased
exploration of novel objects [35]. Apathy may occur in
animals that are kept in barren environments or that have a
perceived sense of lack of control over their environment,
and it is considered an indicator of poor welfare [36].

When assessing apathy in animals, it is important to
consider the normal rhythm of activity of the species to
distinguish apathy-related inactivity from normal levels of
inactivity.
Regurgitation-reingestion (RR)
RR behaviour (RR) has been described in some primates
such as gorillas, bonobos and chimpanzees [37–39]. It has
been suggested that one of the main factors contributing to
RR is the inability to display normal foraging behaviour in
captivity, and therefore RR would be a potentially useful
indicator of behavioural restriction [40]. RR has also been
described in marine mammals. In these species, RR may
cause a loss of body condition, as food is partially lost in the
water after regurgitation (D. Garcia-Párraga, personal
communication, 2015).
Feather damaging behaviour
Some species of birds, particularly Psittaciformes, may
develop feather-damaging behaviour (FDB) in which they
pull out or damage their own feathers. FDB results from a
combination of causes, including medical problems, stress, a
barren environment and lack of opportunity to perform
normal foraging or social behaviour [41].
Changes in the frequency, duration and intensity of
normal behaviours
Sleep
There are several studies in humans and other species
showing that stress reduces sleep duration and quality [42].
Electroencephalography is the most common methodology
to study sleep, at least in laboratory animals, but it is not
feasible in zoo animals. Interestingly, non-invasive obser-
vation of sleep behaviour is a useful measure of stress in rats
[43] and a similar methodology has been used in domestic
and zoo animals. For example, one study showed that
rapid-eye-movement (REM) sleep decreased significantly in
adult giraffes after a stressful event, whereas poor health
seemed to increase REM sleep in newborn giraffes [44].
Feed intake
The effects of stress on feed intake depend on several
factors including the type of stressor and its intensity. In
general, however, severe stress causes a reduction in feed
intake, which may therefore be considered an indicator of
poor welfare. In some cases, however, stress has the
opposite effect [45, 46].
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X Manteca, M Amat, M Salas and D Temple 3
Rumination
Work done in domestic ruminants has shown that stress
reduces rumination [47, 48]. A review of behavioural
responses to stress in sheep concluded that rumination
decreases in several stressful situations such as social
isolation and separation of lamb from the ewe [49].
Rumination time also depends on the type of diet, and
when there is an insufficient amount of fibre, rumination
time will decrease.
Displacement behaviours
Displacement behaviours are behaviours that seem irrele-
vant and inappropriate in the context in which they appear
and are the result of a conflict situation. It has been
suggested that the frequency of displacement behaviours
such as yawning and self-grooming can be used as a welfare
indicator in primates [50]. One of the main difficulties of
using displacement activities as a welfare indicator is that
they may be normal behaviours that bear no relation to the
emotional state of the animal. Therefore, before drawing
conclusions on the welfare of an animal, long-term
recordings of the frequency of displacement behaviours
are needed.
Anticipatory behaviour
Anticipatory behaviour is shown in response to cues that
signal an imminent rewarding stimulus and includes an
increase in activity [51]. The intensity of anticipatory
behaviour is related to the welfare of the animal. For
example, animals that are kept in barren environments tend
to show more anticipatory behaviour than animals kept in
enriched environments [51]. Therefore, the intensity or
duration of anticipatory behaviour has been suggested as a
welfare indicator in a variety of animals, including zoo
animals [52]. One of the problems when using anticipatory
behaviour to assess welfare is that animals in very poor
welfare may also show a decrease in anticipatory behaviour;
this is the case, for example, with animals that are in a state
of chronic stress [51].
Aggressive behaviour
There are two reasons why aggressive behaviour may be a
useful indicator of poor welfare: first, aggressive inter-
actions may cause injury and stress, and secondly, several
negative emotions such as pain, fear, chronic stress and
frustration may cause or at least increase aggressive
behaviour [53–55]. However, aggressive behaviour is part
of the normal behavioural repertoire of all species and it is
by no means easy to decide when aggressive behaviour is
indicative of a welfare problem. The effects of aggressive
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behaviour on welfare will vary depending on its intensity, as
very intense aggressions are likely to cause more severe
stress and injuries than low-intensity aggression. Therefore,
changes in both the frequency and the intensity of
aggressive behaviours should be recorded. For example, a
study on the behaviour of grey kangaroos concluded that
the frequency of aggressive interactions was higher in
captivity than in the wild, but this difference was significant
only for low-intensity aggressions, which are likely to be
less relevant from an animal welfare standpoint [56].
There are some instances where captive wild animals
show forms of aggression, which are very unlikely to be
part of the natural behaviour of the species, as they would
reduce fitness. This is the case, for example, with male
clouded leopards, which may attack and even kill sexually
receptive females [57]. Although the causes of this behav-
iour are not clearly understood, it has been suggested that
stress may play a role (personal communication: Fernando
Nájera-Muñoz, 2015) and therefore this ‘abnormal’ form of
aggression could be considered an indicator of poor
welfare.
Play behaviour
Play behaviour has been proposed as a positive indicator of
welfare mainly because it is a pleasurable behaviour [58]
and also because animals will play less if they are sick,
malnourished or stressed [59, 60]. However, in some
circumstances play may increase after a potentially stressful
situation such as weaning [61] and also after a period in
which animals have been unable to play [62]. A further
difficulty is that play may be rarely seen, especially in adult
animals. Despite these limitations, play may be a useful
indicator of good welfare in mammals and birds [60];
although behaviours that could be equivalent to play have
been described in other taxonomic groups, it is uncertain
whether animals other than mammals and birds play [63].
Affiliative behaviour
Affiliative behaviours and, particularly, social grooming,
serve to reinforce social bonds and reduce tension in
groups of animals, and based on this have been suggested as
positive indicators of welfare [59]. One of the problems
when using social grooming to assess welfare is that species
differ in the extent to which they show this behaviour. Also,
the frequency of social grooming may change depending on
several factors such as age, group size and composition, and
reproductive state [59]. A further difficulty is that an
increase in social grooming does not necessarily reflect
good welfare. For example, domestic pigs kept in barren
environments show more social grooming than con-
specifics kept in enriched environments where they can
explore and root [64]. Also, animals confined in a reduced
space may show a high frequency of social grooming simply
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because they interact more often. Finally, in some species
social grooming and affiliative behaviours in general may
be part of the so-called ‘reconciliation behaviours’.
Reconciliation behaviour, defined as an increase in affiliative
behaviour after a conflict between two individuals [65] has
been described in a variety of primate and non-primate
species [66].
Maternal behaviour
Emotions play a central role in maternal behaviour [67] and
there is evidence that negative emotions can cause
abnormal behaviour [68]. For example, stress caused by
social disruption and inadequate housing caused infant
neglect in gorillas [69], and experimental administration of
glucocorticoids to lactating female common marmosets
impaired maternal behaviour [70]. The effect of stress on
maternal behaviour is not restricted to primates: in
rodents, maternal behaviour is impaired in females that
have suffered stress during pregnancy and this appears to be
due to a stress-induced reduction in oxytocin receptors
[71]. On the other hand, however, the effect of stress
during pregnancy on maternal behaviour in domestic sheep
is far from clear [72], and therefore the possibility exists
that species differ in this regard. In some cases, stress may
have more subtle effects on maternal behaviour, including
excessive grooming of the offspring or, in carnivores,
moving the offspring from one place to another too
frequently [73].
Disease prevalence and incidence
Although zoo animals often have the benefits of veterinary
care, in some cases the prevalence of diseases is higher in
captive animals than in their conspecifics living in the wild
[74]. Physical health is an important part of welfare [5, 6]
and therefore prevalence/incidence of injuries and diseases
provide relevant information on the welfare of animals. It is
suggested that diseases that cause pain, pruritus or other
forms of discomfort are particularly relevant from an
animal welfare standpoint, as are multifactorial diseases that
depend to a certain extent on the environment in which the
animal is kept and the animal’s stress response.
One example of medical condition that is very relevant in
terms of welfare is lameness, as it is obviously associated
with pain and is multifactorial in nature. Lameness is rather
frequent in several zoo animals (e.g. [75]) and gait scoring
systems similar to those developed for domestic animals
are available for some zoo species [76]. Integument
alterations and clinical signs of respiratory and digestive
conditions have also been used to assess welfare in
domestic animals [77], and they are likely to be useful in
many zoo species as well. Dental problems are very
frequent in some taxonomic groups such as bears [78],

and are likely to have a significant impact on welfare as they
are painful and may interfere with normal behaviour [29].
Life span
Reduced life expectancy indicates that the animal has
suffered stress and that its welfare has been poor [8]. In
zoo animals, life span has been used to study differences
between species in their response to captivity [79, 80]. For
example, females of browsing ruminants kept in zoos have a
lower relative life expectancy (defined as the ratio between
average life expectancy and the record longevity of the
species) than females of grazing species, and this may be due
to the difficulties faced by many zoos to provide an
adequate diet to browsing animals [80].
Another potential use of life span studies is to identify
factors that may decrease the welfare of zoo animals [81].
For example, it has been found that life expectancy of Asian
elephants (Elephas maximus) is negatively affected by
transferring animals from one zoo to another [81].
Although studies using life span and other similar
indicators (such as relative life expectancy) have provided
useful information on the welfare of zoo animals, they have
some important limitations. First, life span is not useful to
assess the current welfare status of a given individual or
group of individuals as differences in life span are likely to
reflect past conditions. For example, work on African
elephants (Loxodonta africana) concluded that life expect-
ancy of zoo elephants had increased during the last years of
the study [81]. A further problem is to find a reference
value for a given species. In the above study on life
expectancy of elephants, the authors compared the
average life span of zoo African elephants with that of
elephants living in the Amboseli National Park and found
that zoo elephants had a significantly shorter life expect-
ancy than elephants living in the wild [81]. It could be
argued, however, that different populations of wild
elephants may have different life expectancies and thus
selecting a given population to obtain a reference value may
affect the conclusions of the study. Finally, it is important to
remember that a long life span is not necessarily equivalent
to good welfare, as a very old animal may still have a poor
quality of life.
Body condition
Significant weight loss or poor body condition often
indicate the existence of a disease or that the animal is
unable to meet its nutritional requirements either because
the diet is inadequate or the animal cannot successfully
compete with other individuals for access to food.
Alternatively, obesity, which is a rather common problem
in some zoo animals, can have adverse effects on health and
may be caused by lack of exercise [82]. Inadequate body
condition should therefore be considered a welfare
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X Manteca, M Amat, M Salas and D Temple 5
indicator. Body condition scoring systems have been
developed for several species of zoo animals (e.g.
[83, 84]). In some cases the scoring systems have been
validated with an independent measure, such as measure-
ment of body fat with ultrasound [85].
Physiological parameters
Long-lasting or intense stress is a welfare problem [5].
Stress involves the activation of the hypothalamic-pituitary-
adrenal (HPA) axis, which in turn results in increased
secretion of glucocorticoids. Therefore, the concentration
of glucocorticoids (cortisol or corticosterone, depending
on the species) or their metabolites has been used to assess
animal welfare. Glucocorticoids or their metabolites can be
measured in various samples, including plasma, saliva,
faeces, hair and feathers [86]. Although potentially inter-
esting, measures of the HPA axis activity are not without
problems [86, 87]. For example, blood sampling itself may
cause stress and change the plasma concentration of
glucocorticoids. Saliva sampling may be less stressful for
the animal than blood sampling, and although it requires
training the animal so that it gets used to the sampling
procedure, it has been successfully used in several species
[88, 89]. Plasma and saliva concentration of glucocorticoids
show a circadian rhythm and ideally samples should be
taken at the same time of the day if comparisons are to be
meaningful. Both plasma and saliva concentrations of
glucocorticoids measure acute stress.
The concentration of glucocorticoid metabolites in
faeces has been successfully used in several species, but
the nature of the metabolites, which are excreted in faeces
and their concentration in faecal samples varies across
species [90, 91]. The excretion of cortisol metabolites in
faeces does not occur immediately after the animal
perceives the stressor, and the time lag ranges from a few
hours to more than 1 day, according to the digestive transit
time of each species [90, 91]. Finally, the concentration of
cortisol in hair or feathers is potentially a very interesting
measure of chronic stress in mammals and birds [92, 93].
Most studies have used measures of HPA axis activity to
assess welfare deal with mammals or birds. However, levels
of glucocorticoid can be useful in other taxonomic groups.
For example, levels of corticosterone have shown to be
reliable indicators of stress in reptiles. Corticosterone can
be measured in plasma [94] and faeces [95] to assess acute
stress, and in keratinized tissues such as snake sheds [96]
and turtle claws [97] to determine chronic stress. Similarly,
cortisol has been used to study fish welfare [98], whereas
corticosterone levels in blood and corticosterone metab-
olite levels in urine can be measured to study stress in
amphibians [99]. Interestingly, a non-invasive technique to
measure water-borne glucocorticoids in fish and amphi-
bians has been developed [99].
It is important to bear in mind that the activity of the
HPA axis may increase in situations that are far from being
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unpleasant to the animal, such as mating or exposure to a
new environment that elicits exploratory behaviour [87].
Also, studies in humans have shown that negative emotional
states such as depression and anxiety may not cause an
increase in cortisol levels [100]. Therefore, HPA axis
activity should not be used as the only measure when
assessing the welfare of the animals, and studies combining
behavioural observations with measures of glucocorticoid
levels are likely to provide more relevant information (e.g.
[101]).
Other potentially interesting physiological measures of
zoo animal welfare are oxytocin concentration, heterophil:
lymphocyte ratio and plasma concentration of acute phase
proteins. Oxytocin is involved in the control of positive
social interactions and contributes to reducing the stress
response, and its concentration in urine has been used as a
positive indicator of welfare [102].
The ratio between the number of heterophils and
lymphocytes has been frequently used as an indicator of
stress in birds as both exposure to a stressor and
corticosterone administration increase it [103]. However,
at least in some circumstances, birds exposed to a very
stressful situation may show the opposite change [104].
The plasma concentration of acute phase proteins varies
as a result of tissue injury or inflammation and has been
used in several zoo animals to assess health problems
[105, 106].
Telomere length
Telomeres are protein-DNA caps that protect the end of
chromosomes. Several studies have shown that exposure
to chronic stress may reduce telomere length [107].
Similarly, social stress caused by individual housing seems
to decrease telomere length in African grey parrots
(Psittacus erithacus) [108]. If further studies show a similar
effect in other species, telomere length could be a useful
measure of chronic stress in long-lived, social species such
as elephants, dolphins and some primates. However, more
information is needed on the genetic and environmental
factors that may affect telomere length in different species
before this parameter can be used to assess welfare.
Keeper ratings
Keepers can provide useful information on the welfare of
the animals they are familiar with by observing their overall
behaviour and demeanour. This qualitative, holistic assess-
ment of welfare based on the subjective impressions of
observers was initially developed for farm animals and is
now an important element in many welfare assessment
protocols used in domestic species. In this methodology,
known as ‘Qualitative Behavioural Assessment’ or QBA,
several observers rate the animals to be assessed on a
number of descriptors such as ‘happy’, ‘bored’, ‘relaxed’,
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‘tense’, etc. It has been shown that the results of QBA have
a high inter-observer reliability and are correlated with
quantitative measures of welfare [109]. A similar approach
can be used in zoo animals and it has been shown that
zoo keeper ratings also have a high inter-observer-reliability
and are correlated with quantitative measures of welfare,
both physiological and behavioural. In summary, and
although more research is needed, it seems that keeper
ratings may be extremely useful to assess zoo animal
welfare, particularly considering the time constraints faced
by zoo staff [3].
Conclusions
This review shows that there is a significant body of
information on animal-based indicators to assess the
welfare of zoo animals. It is also generally agreed that
indicators of good and bad welfare should be used, and
that both the physical health and the affective state of the
animals must be considered when assessing their welfare.
Although most welfare indicators commonly used to
assess welfare of zoo animals are negative indicators,
positive indicators, such as play behaviour, affiliative
interactions and oxytocin, deserve particular attention so
that an approach to welfare evaluation that goes beyond the
avoidance of suffering and considers positive emotions can
be taken.
It is suggested that there are two areas that deserve
particular attention in further research: the development of
zoo animal welfare assessment protocols and the identifi-
cation of indicators to assess the welfare of animals other
than mammals and birds.
Although there are many potentially useful welfare
indicators that can be used in a variety of species or
taxonomic groups, all indicators have methodological
limitations. Also, as mentioned in the introduction of this
report, animal welfare is a multi-dimensional concept that
includes the physical and mental health of the animals as
well as their behaviour, and there is no single indicator that
can provide all the information needed to assess animal
welfare [8]. Consequently, several indicators should be
used to assess welfare and they should be selected based on
the species’ natural history and its most common welfare
problems. Additionally, potential indicators should be
checked for validity, reliability and feasibility. Selected
indicators should then be combined into an assessment
protocol. Several animal welfare assessment protocols have
been developed for domestic species, particularly farm
animals. Among them, the Welfare Quality® protocols
could be particularly useful. The Welfare Quality® proto-
cols include mainly animal-based indictors grouped under
four principles of welfare (good feeding, good housing,
health and appropriate behaviour). Each principle includes
several criteria and each criteria is assessed through a
number of indictors tested for validity, reliability and
feasibility [110]. The Welfare Quality® protocols are

potentially useful for a variety of species [111] and have
been used to assess the welfare of farmed foxes and mink
[112]. More recently, they have been used to develop a
welfare assessment index for captive bottlenose dolphins
(Tursiops truncatus) [84] and work is now in progress to
develop similar protocols for African elephants [113, 114]
and Dorcas gazelles [115]. Clearly, a similar exercise should
be done for as many zoo species as possible.
With a few exceptions (e.g. [116, 117]) most papers on
the assessment of welfare of wild animals in captivity, deal
with mammals or birds. This is unfortunate as many zoos
keep a large number of species belonging to other
taxonomic groups, particularly reptiles, fish and amphi-
bians. For some of these species, zoos are expected to play
a key conservation role. Also, there is evidence that animals
other than mammals and birds may have welfare problems
when kept in zoos. For example, a study has shown that
several species of lizards have a significantly lower life
expectancy in zoos than in the wild [117]. It is therefore
urgent to identify science-based indicators for reptiles, fish
and amphibians.
Acknowledgements
I would like to thank Conrad Enseñat, Daniel García, Hugo
Fernández, Jesús Fernández, Eva Martínez and Sergio
Tejedor for sharing their knowledge on zoo animal behav-
iour and welfare.
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