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Zoo Biology 29 : 237– 255 (2010)
How Should the Psychological
Well-Being of Zoo Elephants be
Objectively Investigated?
Georgia J. Mason
1
and Jake S. Veasey
2
1
Canada Research Chair in Animal Welfare, Animal Science Department,
University of Guelph, Guelph, Ontario, Canada
2
Department of Animal Management and Conservation, Woburn Safari Park,
Woburn, Bedfordshire, United Kingdom
Animal welfare (sometimes termed ‘‘well-being’’) is about feelings – states such as
‘‘suffering’’ or ‘‘contentment’’ that we can infer but cannot measure directly.
Welfare indices have been developed from two main sources: studies of suffering
humans, and of research animals deliberately subjected to challenges known to
affect emotional state. We briefly review the resulting indices here, and discuss
how well they are understood for elephants, since objective welfare assessment
should play a central role in evidence-based elephant management. We cover
behavioral and cognitive responses (approach/avoidance; intention, redirected
and displacement activities; vigilance/startle; warning signals; cognitive biases,
apathy and depression-like changes; stereotypic behavior); physiological
responses (sympathetic responses; corticosteroid output – often assayed non-
invasively via urine, feces or even hair; other aspects of HPA function, e.g.
adrenal hypertrophy); and the potential negative effects of prolonged stress on
reproduction (e.g. reduced gametogenesis; low libido; elevated still-birth rates;
poor maternal care) and health (e.g. poor wound-healing; enhanced disease rates;
shortened lifespans). The best validated, most used welfare indices for elephants
are corticosteroid outputs and stereotypic behavior. Indices suggested as valid,
partially validated, and/or validated but not yet applied within zoos include:
measures of preference/avoidance; displacement movements; vocal/postural
signals of affective (emotional) state; startle/vigilance; apathy; salivary and
urinary epinephrine; female acyclity; infant mortality rates; skin/foot infections;
Published online 9 June 2009 in Wiley InterScience (www.interscience.wiley.com).
DOI 10.1002/zoo.20256
Received 8 August 2008; Revised 21 April 2009; Accepted 5 May 2009
Grant sponsor: NSERC.
Correspondence to: Georgia J. Mason, Canada Research Chair in Animal Welfare, Animal Science
Department, University of Guelph, Guelph, Ontario, Canada N1G 2W1. E-mail: gmason@uoguelph.ca
rr
2009 Wiley-Liss, Inc.
cardio-vascular disease; and premature adult death. Potentially useful indices that
have not yet attracted any validation work in elephants include: operant
responding and place preference tests; intention and vacuum movements; fear/
stress pheromone release; cognitive biases; heart rate, pupil dilation and blood
pressure; corticosteroid assay from hair, especially tail-hairs (to access endocrine
events up to a year ago); adrenal hypertrophy; male infertility; prolactinemia; and
immunological changes. Zoo Biol 29:237–255, 2010. r2009 Wiley-Liss, Inc.
Keywords: preference; motivation; cortisol; stress; welfare; zoos
INTRODUCTION
Ensuring the well being of zoo elephants is challenging in terms of husbandry,
cost and public perception. Objectively quantifying elephant welfare also represents
a considerable challenge. Here, we review how welfare is assessed scientifically, via
behavioral and physiological variables validated and well-used in farm and
laboratory animals. We discuss what is known about them for elephants, and
consider the work yet needed to improve the objective assessment of elephant
welfare. A companion paper [Mason and Veasey, submitted, this volume] reviews the
few studies that have used these indices in a way that helps evaluate the population-
level well being of zoo elephants.
WHAT DO WE MEAN BY WELFARE?
Welfare relates to an animal’s affective (colloquially, ‘‘emotional’’) state: what
it feels. Our use of this word is equivalent to the term ‘‘well-being’’ [see e.g. Brown
et al., 2008], as we use these inter-changeably in this paper. Good welfare means
experiencing positive emotional states, while poor welfare involves severe or
prolonged suffering [e.g., Dawkins, 1990; Mason and Mendl, 1993; Brown et al.,
2008]. Clarifying what welfare is not helps augment this definition. First, health and
welfare are not equivalent; welfare can affect health, as reviewed below and poor
health can also affect welfare, if it involves pain or nausea. However, health issues
without such effects (e.g., a tumor the animal cannot feel; a latent, quiescent virus; or
a potentially painful condition treated effectively with analgesics) do not affect
welfare, at least at that time. Second, welfare is not about simple genetic fitness.
While poor welfare can decrease reproductive output (as reviewed below), this is not
always the case: it would be incorrect, for instance, to assume that all farmed
livestock have good welfare simply if reproducing productively. Third, good well-
being is not about mimicking all aspects of natural life. Performing certain natural
activities may be important, but others may be relinquished harmlessly when human
provisioning and protection render them obsolete [e.g., Veasey et al., 1996a,b].
Fourth, welfare does not necessarily correspond to the intentions of the animal’s
human carers: captive animals can have good welfare despite indifferent keepers, or
poor welfare despite keepers caring deeply. Finally, death must be differentiated
from well-being. How and why death occurs is relevant to welfare, since this may
involve suffering (see below). However, loss of life per se does not imply poor
welfare: death involves the cessation of brain activity, rendering suffering impossible;
death can also be humane (the aim of ‘‘euthanasia’’).
238 Mason and Veasey
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If welfare is about how animals feel, then in the absence of a common
language, how do we investigate it objectively? Subjective experiences and feelings
are inaccessible (the so-called ‘‘Other Minds’’ problem), so to assess them we use
indirect indicators. When evaluating welfare in other humans, we use both learned
language and innate signals (smiling, crying, etc.), whose affective correlates we
understand from our own experiences. These indices generally serve us well.
However, they can be challenging or unreliable in nonverbal humans like babies or
the profoundly disabled: such cases may require measuring heart-rate or other
physiological changes validated (as discussed below) as indices of affect. When
evaluating well-being in other species, even greater challenges occur: reading alien
signals (ear-flapping, growling, etc.); assessing physiological changes without
inducing handling/sampling stress; distinguishing valence (the positive/negative
nature of emotions, central to well-being) from mere arousal (alertness and activity,
which can increase in positive as well as negative situations); and last but not least,
interpreting all findings without anthropomorphism, bias or circular reasoning.
Certainty about conscious experiences in other animals is thus impossible; and so-
called ‘‘welfare measures’’ are merely indices from which we make only inferences.
But what are these indices and where do they originate? Most come from two
well-established fields:
1. Clinical research in humans with physical or mental problems: Verbal reports from
suffering people (enduring stressful events like war, divorce, or bereavement;
suffering from emotional disorders such as anxiety and depression; or
experiencing physical harm that causes pain or nausea) are compared with
changes in biological functioning (e.g., cognitive changes, hormonal profiles, or
immunological changes), to yield potential biological correlates of affective state.
2. Animal-based physiology and neuroscience research: To investigate human clinical
conditions (e.g. anxiety and depression), laboratory animals are deliberately
exposed to events believed to cause stress, fear, sickness, or pain, and/or have
such suffering experimentally mitigated via analgesic or anxiolytic drugs.
Behavioral and physiological changes again yield candidate indices of the
affective states induced/redressed by these treatments.
Both these fields tend to yield similar indices, providing a range of potential
tools, as reviewed next, for assessing animal well-being.
HOW TO ASSESS ELEPHANT WELFARE?
Here, we summarize key welfare indices, especially those sensitive to
psychological well-being (stress, frustration, and anxiety/fear), as detailed in many
stress and welfare texts [e.g., Archer, 1979; Dawkins, 1980, 1990; Mason and Mendl,
1993; Broom and Johnson, 1993; Toates, 1997; Clubb and Mason, 2002, p. 7; Brown
et al., 2008; further references are given below where they refer to additional
specifics]. We cover behavioral and psychological changes (A), then physiological
changes (B), and, finally, the consequences of physiological changes for reproduction
and health (C). We also review species-specific research on these indices in elephants.
Our aim is to evaluate the usefulness of various indices for assessing zoo elephant
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welfare, recommend how best to use them in practice, and highlight potentially
valuable indices that have been overlooked.
Behavioral and Psychological Changes
Behavioral changes and the underlying CNS processes (e.g., appraisal,
decision-making, and learning) are central to welfare assessment because often
inherently related to pleasure, fear, and other feelings.
Preference and avoidance
Stimuli or events that decrease welfare are typically avoided, while stimuli or
events that increase welfare are typically sought out. This can occur via unlearned
responses (e.g., approach), or learned ones such as performing an arbitrary operant
task (e.g., lever-pressing) or moving to specific locations associated with reward
(‘‘conditioned place preference’’). The more important a resource, the more effort is
generally devoted to gaining it: thus animals typically work harder (travel farther,
overcome greater obstacles, lever-press faster, etc.) for food and water than for non-
essential resources, especially when deprived. Such behavioral responses are
intimately related to the value of different stimuli and experiences: many argue
that the very functions of emotions are to control motivation (goal-directed, effortful
aspects of behavior) and promote learning [e.g., reviewed by Dawkins, 1990].
Preference tests have thus often been used to reveal what animals choose for
improved well-being. For example, chickens prefer larger cages with a substrate to
smaller cages with wire floors [Dawkins, 1983], while naturally semi-aquatic
American mink will push door-weights as heavy as those they will push to gain
food, to reach water in which they can swim and ‘‘head-dip’’ [Mason et al., 2001].
Negative stimuli can be evaluated too; for example, the avoidance of potentially
noxious gasses can be assessed [Cooper et al., 1998; Jones et al., 2003], while the
aversiveness of pain to lame poultry has been revealed by their selection of food
dosed with analgesics over unadulterated food [e.g., Danbury et al., 2000]. Thus,
investigating whether stimuli or experiences induce learning, and quantifying the
efforts animals make to reach or avoid them, can be very useful for identifying and
ranking their affective valence.
Issues to be aware of when applying such techniques include animals requiring
time to experience and learn about the positive or negative effects of the stimuli on
offer. In addition, preference data may need interpretation: threatening stimuli can
occasionally elicit approach because of the need to gain information about potential
danger (e.g., ‘‘predator inspection’’ by prey species); and, furthermore, when animals
interact with a rewarding resource, the stimuli elicited by it (its sounds, odors, etc.)
and experience gained by interacting with it, may enhance or even create a
motivation for it—without such effects, ‘‘out of sight’’ could well have been ‘‘out of
mind.’’ Thus, preference for environmental enrichments, say, reveals the benefits of
adding them to an enclosure and the welfare implications of removing them once
they have been enjoyed, but does not prove that animals that have never experienced
such enrichments are suffering [Warburton and Mason, 2003].
Preference and avoidance measures are likely very useful for elephant welfare
assessment. Studies of wild African elephants’ ranging behavior certainly reveal
clustering around important resources like water [Chamaille
´-Jammes et al., 2008],
and the avoidance of potential threats or wastes of energy. Thus, they show
240 Mason and Veasey
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avoidance of roads [e.g. Blake et al., 2008] and of other areas or signs of human
disturbance [Slotow, 2002; Blom et al., 2004]; they avoid walking uphill [Wall et al.,
2006; Edkins et al., 2008; see Limin and Li, 2005 for similar findings for Asian
elephants]; and they flee from the sounds of enraged bees [King et al., 2007], from
hunts [Burke et al., 2008], and even from the odors of ethnic groups, Masai, who
sometimes kill them [Bates et al., 2007; the sight of distinctive red Masai clothing, in
contrast, elicits approach and attack]. In zoos, however, studies of preference or
avoidance have been little used as yet [Mellor et al., 2007 give one preliminary
example], but they could potentially be very valuable. For example, place preference
paradigms could be used to investigate whether elephants dislike being shackled at
night, whether they find some keeper contact rewarding (perhaps even the odors/
clothes of keepers with different handling styles could be presented), and to address
many other topical welfare issues. In addition, operant approaches could be used to
evaluate potential positive and negative experiences and their importance to zoo
elephants. If slopes are avoided, perhaps ramps of varying steepness could also be
used as experimentally imposed nonoperant costs, to assess efforts elephants are
prepared to make to reach/avoid different resources or stimuli [Schulte et al., 2007
review some other non-operant barriers or obstacles that could potentially allow
evaluation of motivations to approach/retreat].
Other behavioral measures related to preference, avoidance and other motivations
Tendencies to avoid threatening stimuli can be used in a quite different way in
welfare assessment. For one, avoidance responses (e.g., ‘‘startle’’) can be valuable for
assessing state, not just for quantifying the aversiveness of particular stimuli, since
increased tendencies to avoid novel, standardized threats reflect increased underlying
anxiety. These we review in detail in the following section. (Decreasing tendencies to
avoid familiar, repeated stressors may in contrast indicate ‘‘learned helplessness:’’ see
‘‘Apathy and depression-like changes,’’ below.) In addition, frustrated motivations
(e.g. thwarted desires to approach or avoid stimuli or to engage in other activities)
can cause other behavioral responses useful in welfare assessment: ‘‘intention
movements,’’ where animals attempt to reach a relevant resource despite repeated
failure; ‘‘redirected’’ and ‘‘vacuum’’ activities, where inappropriate stimuli are used
as outlets for motivation (e.g., mating with inanimate objects); and ‘‘displacement
activities,’’ where a conflict between two incompatible motivations induces irrelevant
activities like grooming. These responses can thus help reveal an animal’s affective
state. Furthermore, if repeated and sustained, these movements can potentially give
rise to stereotypic behaviors—abnormal behaviors reviewed in more detail below.
Free-living African elephants certainly seem to display distinctive displacement
activities [reviewed and illustrated in Poole and Granli, 2009]. In an ambivalent,
slightly apprehensive animal, apparently unsure of what action to take, these include
trunk-twisting (the trunk-tip being twisted back and forth), foot-swinging (raising
and tentatively intermittently swinging the foreleg, or occasionally the hind leg), and
‘‘touch face’’ (touching the trunk to the animal’s own face, mouth, tusk, or temporal
gland). Displacement grooming and displacement feeding also occur, activities
characterized by situational and functional inappropriateness. For instance, caught
between two incompatible motivations (e.g. fleeing and fighting), wild African
241Welfare Indices for Elephants
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elephants may begin to throw dust or grass onto themselves, or pluck at vegetation
without ingesting it. Such indices seem not, however, to have been used in studies of
captive elephant well-being.
‘‘Startle’’ and other responses to potentially threatening stimuli
Many tests of fear, especially those conducted on rodents to investigate
anxiety, involve assessing reactions to a standardized ‘‘probe’’ stimulus that is
inherently mildly aversive [e.g., Crawley, 2007]. Such stimuli include open, brightly
lit areas or novel objects, which rodents typically avoid. Importantly, such avoidance
responses increase in individuals previously exposed to treatments that increase
anxiety (e.g., social isolation; predator odors), but decrease after anxiolytic drugs.
Another innate avoidance response used to assess anxiety is the ‘‘startle’’ induced by
a sudden, standardized sound or touch; again, animals previously exposed to
stressors show more exaggerated startle responses than control animals, while
anxiolytic drugs reduce these responses. These anxiety indices are standard in
biomedical research using rodents; have recently been applied to rodent welfare
research; and have just started to be used elsewhere, for example, with farmed
ungulates. On the contrary, their application in zoos has been negligible, with no
known usage in elephants as yet, neither to assess what stimuli cause
fear, nor—via the use of probe stimuli—to assess background anxiety.
Signs of increased vigilance such as ‘‘head-up’’ scanning postures or eye
widening [which probably functions to increase peripheral vision; Susskind et al.,
2008] may also be useful welfare indicators. For example, eye-widening that shows
the whites is a well-validated fear/distress index in cattle [e.g., Sandem et al., 2002;
Core et al., 2009], again to both identify negative stimuli and, by using standardized
‘‘probe’’ stimuli, assess underlying anxiety. Eye-widening revealing the whites
similarly occurs in wild African elephants when alarmed or anxious [Poole and
Granli, 2009]. However, it is also seen during intense social interactions and excited
play [Poole and Granli, 2009]. This suggests that while eye-widening could be useful
in elephant welfare assessment, one must control high levels of general arousal since
this is a potential confound (an issue returned to below). Other behavioral signs of
alarm/vigilance in wild African elephants include freezing, scanning, and smelling
the air [O’Connell-Rodwell et al., 2007].
Signals to conspecifics
Group-living animals and mothers and infants often signal to each other about
emotionally significant events, particularly danger but also sometimes seemingly to
convey relaxation (e.g., cats purring). Such signals are typically species-specific, and
can be visual, auditory, or olfactory. Examples used in welfare assessment include
vocal pain responses in piglets [Weary et al., 1998] and chromodacryorrhoea, a
stress-related red tear-like secretion, in rats [Mason et al., 2004]. Caveats when using
animal signals in welfare assessment include the risks of anthropomorphism faced
with signals that look like our own (e.g., liquid running from the eyes), and
conversely our insensitivity to other animal signals (such as sounds at frequencies
our ears cannot detect, and odors). Another caveat is that signals are typically
problem-specific (e.g. signaling-specific states like hunger or fear, but not ‘‘general
poor welfare’’).
242 Mason and Veasey
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Wild elephants display many signals that seem affectively significant, including
diverse trunk and ear postures [e.g. Poole and Granli, 2009]; for example ‘‘head low’’
and ‘‘ears-back’’ postures occur during appeasement, while ‘‘trunk curled under’’
occurs during apparent alarm/apprehension. Liquid ‘‘temporin’’ flow from the
temporal glands has also anecdotally been linked with excitement and high arousal,
including stressful situations. Slotow [2002] even suggests that temporin flows when
wild elephants are disturbed by humans, though not all agree, most interpreting it as
a socio-sexual signal [e.g., Weibull and Eriksson, 1998; Sukumar, 2003].
These postural, vocal, and other signals are doubtless used in an informal,
everyday way by perceptive elephant keepers. However, their validation for and
formalized application to elephant welfare assessment seems undeveloped. One
potential exception is a recent acoustic analysis of zoo animals’ rumble vocalizations,
made during apparently positive and negative social interactions [Soltis et al., 2009].
These differed measurably, particularly in energy content. This study could not
disentangle valence from mere arousal, but nevertheless if developed, this type of
research could yield validated indices of affect for future use.
Note that not all signals of warning, fear, or distress made by elephants are
readily detected by humans. For example, some alarm calls of African elephants are
infrasonic [Moussaieff Masson and McCarthy, 1995; O’Connell et al., 2007], and so
hard to monitor without specialized equipment. Olfactory signals are also hard to
assay [though the effect of, say, urine from stressed or unstressed animals on
conspecific behavior can be used as a ‘‘bioassay:’’ see Mason et al., 2009].
Cognitive biases
Humans in negative moods (e.g. sad or scared), or with clinical depression (see
below), show pessimistic skews in how they perceive and classify events: in
particular, neutral or mildly negative events are judged as being more negative or
threatening than they are by people in positive moods. Similar ‘‘cognitive biases’’
occur in animals [e.g. Harding et al., 2004; Burman et al., 2008; Matheson et al.,
2008]. Thus in one study [Harding et al., 2004] rats were trained that if they heard a
sound at a certain pitch, food would be delivered if they pressed a lever, while if they
heard a sound of another pitch, the lever would instead emit a blast of aversive noise.
These trained rats were then housed in two ways: in large enriched cages or in
standard cages made stressful by regular disruption. The two groups were re-exposed
to the two sounds, but also to a range of probe sounds of intermediate pitch.
Enriched rats treated these ambiguous sounds ‘‘optimistically,’’ as though predicting
a lever-delivered treat, but stressed rats treated them ‘‘pessimistically,’’ as if signaling
that lever-pressing would be punishing [see also Burman et al., 2008; Matheson et al.,
2008].
Quantifying cognitive bias is valuable because subject to minimal confounds
(e.g. not influenced by arousal/activity, like many other indices of affect); because
negative biases potentially cause as well as reveal welfare problems; and because
positive bias is a rare example of an index of good well-being. Cognitive bias has not
yet been used to assess zoo animal well-being, but could be ideal, especially for
elephants whose learning abilities should facilitate training in the relevant tasks.
Such approaches might address whether new arrivals to a herd have negative
cognitive biases compared with more settled members; whether removing a mother’s
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calf leads to negative cognitive bias; whether large enriched enclosures induce
positive cognitive biases; and many other relevant welfare questions.
Abnormalities in behavior and brain function I: Apathy and depression-like changes
As well as negative cognitive biases, humans with depression show reductions
in activities that require motivation or usually cause pleasure, e.g., personal care,
work, exercise, social interaction, and sexual activity. Similarly, low levels of activity
and reduced libido are often observed in rodents subject to repeated stressors (indeed
stressors are applied to rodents in order to ‘‘model’’ human depression in biomedical
research). Low levels of activity, poor self-grooming, low libido, and a lack of
interest in maternal care are likewise often observed in captive animals, and are
sometimes labeled ‘‘apathy.’’ However, typically, it is hard to confidently classify
these changes as truly depression-like; validation would include evidence of
concomitant changes in cognitive bias (see above) or endocrine function (especially
in the HPA axis: see below), and the reversal of these effects with antidepressants. In
laboratory animals experimentally exposed to repeated stressors that they cannot
escape from (e.g. unavoidable electric shock), a paradoxical lack of avoidance of the
harmful stimuli can occur too. Termed ‘‘learned helplessness,’’ this passivity is also
held to mimic aspects of human depression. However, in zoo animals showing
superficially similar effects, it would be hard to tell an individual that has successfully
habituated (so no longer finding the stimuli aversive), from one with true ‘‘learned
helplessness:’’ further validatory data (e.g. the cognitive, endocrine, and pharma-
cological approaches listed above) would be required.
Thus overall, when captive animals are labeled ‘‘apathetic’’ or ‘‘depressed,’’ the
term is potentially valid—but in practice applied very subjectively. This caution
noted, there have been striking, if anecdotal, accounts of elephants becoming very
quiet and inactive after social separation [Moussaieff Masson and McCarthy, 1996]
or ‘‘trauma’’ [Derby, 2008]. Ill elephants are also said to move their trunks, switch
their tails and flap their ears less than healthy animals [Chatkupt and
Sollod, 1999, citing Schmidt, 1986]. Furthermore, in a survey of Thai working
elephants [Chatkupt and Sollod, 1999], elephants that moved ‘‘intermittently’’ were
found to have poorer body condition than those that moved ‘‘frequently,’’ as were
those described as ‘‘dull’’ or ‘‘quiet.’’ While such categorization was subjective and
confounds abounded (for instance poor body condition and little movement were
both seen in animals with insufficient shade), attempts to validate and utilize such
behavioral indices could well prove valuable in future welfare studies.
Abnormalities in behavior and brain function II: Stereotypic behavior
Abnormal repetitive behavior, such as stereotypic pacing, is common in zoos
[e.g., Mason et al., 2007]. It has long been used in welfare assessment for two reasons:
it often originates from intention movements and other behavioral signs of frustrated
motivation (see above); and meta-analyses show that it is most evident in treatments
or environments that induce other signs of poor well-being [Mason and Latham,
2004; Mason et al., 2007]. Indeed, stereotypic behaviors have recently been formally
defined as ‘‘repetitive behaviors induced by frustration, repeated attempts to cope,
and/or central nervous system (brain) dysfunction’’ [Mason, 2006]. This distin-
guishes them from repetitive behaviors that do not indicate poor welfare (e.g., a cat
kneading a comfortable lap, or a dog circling before settling to sleep). Two key
244 Mason and Veasey
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caveats when using abnormal repetitive behaviors to infer well-being are as follows.
First, they may indicate past problems more than current ones [for instance, if they
reflect abnormal brain development during infancy; Mason, 1991; Mason and
Latham, 2004; Mason et al., 2007]. Second, whether groups or individuals with
negligible stereotypic behavior truly have better welfare than those with high levels
depends on what they are doing instead: if they are ‘‘apathetic’’ (see above), hiding,
or immobile due to pain [e.g., Mellor et al., 2007], their welfare may actually be
poorer than that of animals with overt abnormal behavior. Thus empirically, within
populations showing abnormal repetitive behavior, those individuals with the
highest levels often seem to cope best (as assessed via other welfare indices) with the
sub-optimal environments in which they live [Mason and Latham, 2004].
Typical abnormal repetitive behaviors in zoo elephants are swaying/weaving,
head-nodding, and sometimes pacing; the trunk may be moved in a repetitive and
unvarying way too [reviewed by Clubb and Mason, 2002; Harris et al., 2008]. In a
recent survey of all UK zoos, side-to-side swaying/weaving was indeed the most
common across this population, while the rarest form involved repeatedly rubbing
tusks on bars and ropes, wearing grooves into the ivory [Harris et al., 2008]. Are
these repetitive behaviors stereotypic? At least some are increased by treatments like
tethering [e.g., Friend, 1999; Kurt and Geraı
¨, 2001], or stressors like the onset of
parturition [Szdzuy et al., 2006] or approach of a dominant conspecific [Derby,
2008], and so it seems reasonable to class these responses in elephants as true
stereotypic behaviors. However, in a few cases they may reflect past problems more
than present; for example, zoo elephants originating from circuses are particularly
prone to this behavior [Harris et al., 2008]. This issue acknowledged, several studies
have used stereotypic behavior to investigate zoo elephant welfare, including in
animals who have lived in zoos all their lives.
Physiological Responses and Their Effects
Behavioral and psychological responses to threats or stressors are supported
(e.g., fuelled) by appropriate changes in underlying physiology. These necessary,
adaptive changes underlie such ‘‘stress responses’’ as racing hearts, dilated pupils,
and so on. These are potentially useful to assess short-term changes in well-being;
furthermore, if activation is prolonged or excessive, harmful side effects can also
occur (reviewed in the following section).
Adrenaline (epinephrine) release and other sympathetic responses
The release of the catecholamines adrenaline (epinephrine) and noradrenaline
(norepinephrine) into the bloodstream from the adrenal medulla is part of the
sympathetic response—a suite of neural and hormonal changes that help optimize
the performance of behaviors needing energy, such as fleeing or fighting. Effects
include increased catabolism, increased heart and respiration rates, increased blood
pressure, and pupil dilation. Catecholamines are secreted during an animal’s normal
activity periods, thus typically displaying a circadian pattern in most species, but are
also elevated by aversive stimuli. Note that parasympathetic activation, sometimes
treated simplistically as an index of calmness, can also play a role in this acute
autonomic stress response, prompting urination and defecation.
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All these are common correlates of acute stress or fear; and in humans with
chronic anxiety, such responses may be elevated for long periods of time. In animal
studies of fear and anxiety, especially rodent-based research, defecation rates are
often recorded, while heart rates may be assessed via surgically implanted devices or
strap-on external heart-rate monitors (the latter used successfully in welfare research
on large domestic ungulates). Furthermore, adrenaline and noradrenaline can be
detected in saliva and urine: noninvasive techniques of inferring plasma levels that
minimize risks of the sampling itself elevating the hormones being measured. The
main caveat when using such indices in welfare assessment is that they are also
sensitive to activity and arousal in general, and so can also increase during
pleasurable behavioral activities, such as playing or copulation. Heart-rate and
blood pressure are also affected by posture (often increasing with lateral recumbency
in large mammals); furthermore, catecholamines are labile and so for valid assay
need rapid deep freezing after collection.
In terms of using the sympathetic responses of elephants in welfare assessment,
adrenaline and noradrenaline levels can be assayed from urine [Dehnhard, 2007],
and adrenaline can also be extracted and assayed from elephant saliva [Exner and
Zanella, 1999]. Dehnhard [2007] successfully showed that urinary catecholamines
were elevated in two cows after being transferred, a presumably acutely stressful
event. Soltis et al. [2009] also used urination/defecation by subordinates during a
social encounter as evidence of negative affective, although this index seems not to
have been formally validated. Heart rates, which typically range between 24 and
50 bpm, can be measured by means of external electrodes [Bartlett, 2006], but seem
not to have been recorded as part of any welfare-oriented study as yet; the same
appears true for blood pressure.
The hypothalamic-pituitary adrenal axis I: Corticosteroid levels
For physiologists, the hypothalamic-pituitary adrenal (HPA) axis is the classic
stress system of the body [see Brown et al., 2008 for a good review]. Glucocorticoids
are secreted by the cortex of the adrenal gland, in response to the release of
adrenocorticotrophic hormone (ACTH) by the brain’s pituitary. The functions of
these hormones includes facilitating the mobilization of energy reserves to prepare
the animal for a response such as fight or flight. Thus, like catecholamines, they show
a circadian pattern that relates to normal activity cycles, but are also elevated by
threat. They complement sympathetic responses, but typically are activated for
longer after a threat and have more diverse secondary effects on other physiological
processes throughout the body.
Assessment of HPA activity in animal welfare work typically involves
measuring ACTH and corticosteroids in the plasma; corticosteroids diffusing into
the urine or saliva (as with adrenaline, concentrations in these fluids track those in
the plasma, while being easier to sample without stress); or corticosteroid
metabolites evident in the feces. Whether urine or feces is the main route for
excreting these hormones varies between species and even sexes [e.g., Touma et al.,
2003 on mice]. Techniques have also been developed recently to assay corticosteroids
laid down in follicles during hair/fur growth. Assaying hair steroids to infer the time-
line of significant past events has long been used in human drug-testing, thanks to
the serial, stable deposition of such compounds along the hair shaft [see Davenport
et al., 2006]. Recently, endogenous corticosteroid deposits have similarly been
246 Mason and Veasey
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assayed in hairs from macaques, cats, and dogs [Davenport et al., 2006; Accorsi
et al., 2008]. Like sympathetic responses, HPA responses sometimes have to be
treated with caution in welfare research because acute elevations in glucocorticoids
can occur during excitement or simple exertion, not just in situations where well-
being is compromised. Corticosteroid outputs also vary with estrus status in
elephants [Oliveira et al., 2008]. A final confound is that, as reviewed in the next
section, levels can sometimes fall with severe or early life stress.
In elephants, cortisol is the key corticosteroid produced by the adrenal [e.g.,
Brown et al., 2008]. Baseline levels, or rapid, brief elevations of cortisol output, may
be detected in both elephant saliva [Dathe et al., 1992; Exner and Zanella, 1999;
Menargues et al., 2008] and urine [Brown et al., 1995]. Baseline levels and longer,
more sustained changes in output may also be detected via metabolites in the feces
[Stead et al., 2000; Wasser et al., 2000; Foley et al., 2001; Ganswindt et al., 2003;
Millspaugh, 2003; and Hunt and Wasser, 2003 for Africans; e.g., Laws et al., 2007
for Asians]. These metabolites peak in the feces approximately 30 hr after a stressful
event. It does not yet seem clear whether urine or feces is the main route for cortisol
metabolite excretion in elephants, nor whether this varies between sexes. Biological
validation of fecal assay techniques in wild elephants includes the increase of cortisol
metabolites with natural stressors like being a subordinate herd member, being
exposed to severe dry seasons, experiencing a thunder storm, or being injured
[Wasser et al., 2000; Foley et al., 2001; Ganswindt et al., 2005; Millspaugh et al.,
2007], and with anthropogenic stressors like being hunted [Burke et al., 2008] or
translocated [e.g., Viljoen et al., 2008]. Fecal cortisol metabolite levels also co-varied
with submissive behavior in one study of zoo elephants [Burks et al., 2004].
A final assay technique with untapped but enormous potential for elephants is
to quantify cortisol trapped in hair. Research in a quite different field has shown that
certain isotopes deposited in free-ranging wild elephants’ tail hairs reliably reflect
their movements and diets over the previous 12 months [Cerling et al., 2006]. Thus, if
cortisol extraction techniques were validated for elephant hair, the long strands from
their tails could potentially be used to assess the impact of events throughout the
previous year, which could be extremely useful for the retrospective investigation of
past experiences (e.g. moves from zoos to sanctuaries, weaning, past changes in herd
composition, etc.).
The HPA axis II: Changes in HPA functioning
In cases of chronic stress, HPA outputs and responsiveness can be chronically
elevated; this can even result in the hypertrophy of the adrenal gland cortex [e.g.,
Terio et al., 2004]. The HPA system can also respond with changes in circadian
patterning (the loss of the normal night-time trough occurs in some humans with
depression), or even with decreased adrenal activity largely due to upregulation of
negative feedback loops within the axis and/or habituation of the adrenal to ACTH
[see also Brown et al., 2008]. Thus, while chronic elevation is a likely sign of severe
welfare problems, unchanged or even reduced activity may also occur, making
interpretation complex and in need of validation by other measures, particularly
ACTH levels, signs that any chronic changes in HPA function have caused lasting
harm (see below), and independent welfare indices.
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Long-term studies of HPA output or changes in circadian patterning seem not
to have been conducted on zoo elephants; there also seems to have been no use of
adrenal size/structure post mortem to assess the merits or demerits of particular
husbandry systems, even though elephant adrenals have been well-studied [Kramer
et al., 1991] and are typically removed during necropsies (cf. AZA standard
protocols).
Negative Effects of Prolonged Physiological Stress
If stress is chronic, health and fecundity may be affected, partly due to direct
effects of over-activation of the endocrine systems involved (e.g., on reproductive
physiology and inflammatory pathways), and partly due to resulting reduced
immune responses to pathogens. Thus, consequences of chronic physiological stress
include immunosuppression (possibly combined with pro-inflammatory states), poor
wound healing, reduced fertility, reduced protein synthesis (e.g., body-mass loss),
chronically elevated blood pressure, gastric ulceration, increased parasite loads,
elevated pathogenicity of opportunistic infections, and even premature death.
Reduced reproductive success
A well-documented effect of chronic stress in humans, research rodents, and
many other species [see reviews by e.g., Wingfield and Sapolsky 2003; von Borell
et al., 2007; Clubb et al., 2009] is reduced fertility. In adult females, this can be
manifest as impaired cycling/reduced estrous periods, low libido, premature
reproductive senescence, reduced conception rates, increased pre-term fetal losses,
prolonged parturitions, smaller birth weights, asymmetrical infant development,
increased offspring stress responsiveness, poor maternal care (or infanticide), and/or
increased infant mortality. Many of these effects stem directly from HPA axis over-
activation, but additional causal factors include stress-induced prolactin elevation
[Sobrinho, 1998, 2003] and, more speculatively, luteolytic stress-activated protein
kinases [as activated by mitogens: Yadav et al., 2001]. Oxytocin, too, is a crucial
reproductive and maternal hormone, especially during parturition and in the early
stages of maternal care, whose release can be inhibited by stress [see e.g., Leng et al.,
1987; Pedersen and Boccia, 2002; Kiecolt-Glaser et al., 2002].
Just as for most welfare indices, reduced fecundity is far from a perfect index
that always indicates negative affect. Factors reducing reproductive rate that are
independent of well-being include obesity and lack of adequate socialization with
opposite sex conspecifics when young. Several such explanations apply specifically to
elephants. For example, Hermes et al. [2004] suggest that the mere lack of breeding
when young accelerates reproductive senescence in these species – although in zoos,
such data are correlational only (not causal), and so do not preclude the possibility
that females that fail to breed when young had subclinical problems even then, only
manifest overtly later in life. Other impediments to elephant reproduction that are
unlikely to reflect poor psychological well-being include: hypocalcaemia [van der
Kolk et al., 2008; Hermes et al., 2008]; poor physical fitness compromising
parturition [Hermes et al., 2008]; dam parity and past experience (including with the
infants of other females); and, critically, restricted access of females to males and
limited mate choice (due to the way cows and bulls are largely kept separate).
248 Mason and Veasey
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Overall, however, these caveats acknowledged, chronic stress remains a
sensible hypothesis to explore, especially when there is evidence of diminished
fecundity not caused by mere single sex groupings. However, thus far there has been
rather little work on the impact of stress on elephant reproduction in captivity. Wild-
caught Asian timber elephants, who experience very stressful ‘‘breaking’’ processes
followed by high mortality rates, have lower fecundity than captive-bred animals
working in the same conditions [Mar, 2007]. Furthermore, in wild African elephants,
females from herds socially disrupted by poaching, show low calf outputs, despite
being in their reproductive prime [Gobush et al., 2008]. However, despite the
research reviewed above on the assessment of HPA activity, and despite preliminary
work to develop assays for stress-activated proteins in African elephants [Bechert
and Southern, 2002], only one laboratory, Janine Brown’s, has investigated possible
links between stress and reproductive success in zoo elephants. So far, Brown’s work
has focused on acyclicity only; it has revealed no significant links between this and
HPA output (although the highest cortisol levels did seem to occur in noncyclers),
but in Africans, acyclicity was linked with elevated prolactin levels that stemmed
from super-normal prolactinemia in about one-third of the noncycling population
[Brown et al., 2004]. As yet, there seem to have been no studies of the possible role of
stress (perhaps acting via prolactin or oxytocin) in the long parturitions, high infant
mortality rates, and other reproductive problems common in zoo elephants. (See also
Mason and Veasey, submitted to this volume, for more detail.)
Increased morbidity and decreased lifespan
In humans, stress causes increased susceptibility to both opportunistic
infections (e.g., oral and gastric ulcers, fungal infections, skin boils, and Herpes
sores) as well as to infectious diseases caught from conspecifics (e.g., colds and
influenza) [e.g. Kiecolt-Glaser et al., 2002, 2003; Danese et al., 2007]. It also impairs
wound healing, and increases the severity and prevalence of noninfectious
pathologies (e.g. cancer and cardio-vascular disease). Similar effects can be seen in
a range of other species [cf. Mikota, 2008; Clubb et al., 2009]. Chronic stress
therefore decreases life expectancy, in species as diverse as rats, humans, and rhesus
monkeys [reviewed by Clubb et al., 2009], the typical pattern being is that stress
shortens mature adult lifespan [e.g., Kiecolt-Glaser et al., 2002; Cavigelli et al., 2005;
see also Mason and Veasey, submitted to this volume, for more detail].
These potential consequences of chronic stress can thus be useful in assessing
animal welfare, not least because they may cause as well as reflect poor welfare.
Potential confounds, however, when using morbidity and mortality data to make
inferences about well-being, include that infection rates/severities do not just reflect
factors intrinsic or endogenous to the individual, but also extrinsic factors too, such
as exposure rates to pathogens and the quality of veterinary care available.
Furthermore, many noninfectious diseases can be affected by diet and exercise as
well as stress; thus lifespan, for instance, can be reduced by a host of other variables,
some of which, like access to ad lib. food and thence excess body fat, may even be
positive for psychological welfare. Mortality rates must thus be viewed as good
barometers of husbandry, but not necessarily of welfare per se. Despite these issues,
if used carefully, data relating to mortality may be useful in zoo welfare assessment
because zoo animals are frequently allowed to reach maximal longevity. Disease
rates could too, if co-occurring with other signs of poor well-being.
249Welfare Indices for Elephants
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In elephants, does stress affect health and longevity? Sikes [1968] reported that
wild African elephants can succumb to cardio-vascular disease. He also argued that
this was caused by stressful over-crowding and habitat degradation, though not all
agree with this interpretation and other measures of stress were not taken from these
animals. In Asian elephants taken from the wild to work in timber camps, stressful
capture and ‘‘breaking’’ is followed by a period of dramatically elevated risk of death
that last for several years [Mar, 2007; Clubb et al., 2008], although the biological
causes of these deaths are unknown. Foley et al. [2001] found a correlation between
corticosteroid levels and conspicuous signs of gastro-intestinal parasites in wild
African elephants. This would be consistent with a link between stress and increased
vulnerability to parasitism, although equally could indicate an increase in stress as a
result of infestation. Finally, in a recent survey of 16 UK zoo elephants, lameness
scores co-varied with fecal corticosteroid metabolite outputs, the lamest animals
showing greatest endocrine signs of stress [Rajapaksha et al., 2006]. Again, this could
be consistent with stress contributing to the etiology of some foot problems, but it
could equally just reflect that pain and disability cause stress (furthermore, this result
does not appear to be reported in Harris et al., 2008’s larger study of this
population). Overall, morbidity and mortality – and potential risk factors like
elevated blood pressure, thymus involution, and poor wound healing – thus could be
affected by stress levels in elephants, just as in other species, but there has been little
in-depth research.
DISCUSSION: AN OVERVIEW OF POTENTIAL WELFARE INDICES FOR ZOO
ELEPHANTS
As we review, several behavioral, physiological, and health-related variables
are used in scientific animal welfare assessment. The best animal welfare research
controls for known potential confounds (e.g. activity levels, time of day, or stage of
estrus cycle); uses indices that are well-validated, and whose strengths and
weaknesses are well-understood; tests clear hypotheses, selecting measures best
suited for the specific questions under study; and typically uses multiple approaches,
because, as we have seen, no one single welfare index is perfect. It is worth noting
that poor quality welfare research, in contrast, fails to control for or acknowledge
confounds or alternative explanations for findings; uses poorly chosen or validated
measures, to test unclear hypotheses (an approach potentially fraught with circular
reasoning); and often relies on just a single measure.
To date, the most thorough scientific welfare research has been done on farm
and laboratory animals. Farm animal welfare assessment has been a research topic
for over 30 years. Laboratory welfare research, although not as venerable, benefits
from the use of laboratory animals as models to study anxiety and depression, such
that well-validated indices of these states abound for these species. Work on zoo
animals, including elephants, lags far behind. However, there has been good work on
some species [e.g., clouded leopards and black rhinos; see Carlstead et al., 1999;
Wielebnowski et al., 2002]. Furthermore, several potential welfare indices have been
well-validated for elephants, in the sense that reliable measurement techniques have
been worked out, the indices have been shown to change in situations generally
agreed a priori to cause stress or other forms of reduced well-being, confounds are
fairly well-understood, and sometimes they have also been shown to co-vary with
250 Mason and Veasey
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other potential welfare indices. This is a cause for optimism. There is thus real scope
for welfare indices to be used in zoos to both monitor and improve the welfare of
specific, known elephants, as well as to follow the farm and laboratory animal model
in collecting data from larger sample sizes to make recommendations that apply
broadly across the population. Some uses of these indices to assess the welfare of zoo
elephants in general are reviewed elsewhere by Mason and Veasey [submitted].
As we also show here, however, many other potentially valuable indices for
elephants still await proper validation – or even any investigation at all. Elephant
welfare indices that have been suggested as valid, partially validated, or validated but
not yet applied in any meaningful way in zoos, include: measures of preference/
aversion; intention, vacuum and displacement movements; vocal/postural signals;
startle/vigilance; apathy; salivary and urinary epinephrine; female acyclity; infant
mortality rates; skin/foot infections; cardio-vascular disease; and premature adult
death. Furthermore, many indices have not yet attracted any study at all in
elephants–despite their great potential value. These include: operant responding and
place preference tests; fear/stress pheromone release; cognitive biases; heart rate,
pupil dilation and elevated blood pressure; corticosteroid assay from hair
(potentially very useful for the retrospective assessment of events months past);
adrenal hypertrophy; male infertility, prolactinemia; and immunological changes.
Does this lack of research matter? After all, for many, scientific approaches to
captive elephant welfare issues will seem painfully pedantic and unnecessary (‘‘Isn’t it
obvious that small concrete enclosures are bad?’’). We argue that the use of scientific
welfare indices has major advantages over just assuming that we ‘‘know’’ what
elephants need for good well-being. First, where there are assumptions about what
elephants need for good welfare based on human perspectives (e.g., ‘‘they have little
to do, therefore boredom must be a source of misery’’), such indices can be used to
test these assumptions objectively. Second, when contrasting opinions exist about
the potential causes of and solutions to welfare problems (e.g., hypotheses about
whether human contact substitutes for interactions with conspecifics, or whether
environmental complexity is an adequate substitute for space), such data could
reveal objectively which viewpoint is correct. Third, where welfare needs are costly to
meet, or in practical terms mutually exclusive (cf. e.g., having large social groups
versus lots of space per animal), such data can help rank which are most important
to provide. Overall, if elephant husbandry is to be evidence-based, and elephants’
own perspectives (rather than human assumptions) are to guide how they are housed
and cared for, then welfare indices like the ones described here need to be validated,
refined, and above all, used. In the following paper [Mason and Veasey, submitted],
we survey what the few such studies to date suggest about zoo elephant well-being at
the population level.
CONCLUSIONS
1. Animal welfare is about feelings – states like ‘‘suffering’’ or ‘‘contentment,’’ which
we cannot measure directly, but can infer from certain behavioral and cognitive
responses, physiological responses, and effects on reproduction and health.
2. All these indices have their pros and cons, and good quality animal welfare
research therefore typically uses multiple, complementary, well-chosen indices to
reduce the risks of confounds.
251Welfare Indices for Elephants
Zoo Biology
3. Currently, there are just two well-validated, commonly used welfare indices for
elephants: corticosteroid outputs (often assayed from feces) and stereotypic
behavior. Both have their limitations.
4. Several other indices have been suggested as valid, partially validated, or
validated for elephants but not yet applied in zoos (for example, measures of
preference/aversion; startle/vigilance responses; salivary and urinary epinephrine;
cardio-vascular disease; some infections), while several further potential welfare
indices have not yet attracted any study at all in elephants (e.g. fear/stress
pheromone release; heart rate and pupil dilation; corticosteroid assay from hair;
adrenal hypertrophy; prolactinemia; immunological changes).
5. We argue that objective welfare indices for elephants need to be better developed,
since they should play a central role in evidence-based elephant management.
ACKNOWLEDGMENTS
Many thanks go to Debra Forthman for her encouragement, patience, and
help with an earlier version of this work; to Janine Brown and two anonymous
referees; to Phyllis Lee for discussions on Sikes’ work in Tsavo; and to Joyce Poole
for access to her unpublished book chapter on elephant signals. Georgia Mason is
funded by NSERC.
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255Welfare Indices for Elephants
Zoo Biology
