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The physiological and behavioural effect of human
handling on trained African elephants (Loxodonta
africana)
Marina Visser
2
ABSTRACT:
Introduction: Domesticated African elephants (Loxodonta africana) are used for elephant-back safaris and
interactions with tourist. The keeping of elephants is currently under debate, since they are highly
intelligent and social animals (Veasey, 2006). Measuring the welfare of these elephants is critical since it
can have serious consequences such as reproductive problems, occurrence of stereotypic behaviour, higher
incidences of aggression and diseases and a higher death rate.
Methods: Faecal glucocorticoid metabolites were analyzed using a validated enzyme immunoassay
(Ganswindt et al, 2003) to assess physiological stress in a sample of trained African elephants at an
elephant-back safari company. These elephants were experiencing daily exposure to and handling by
humans both trained handlers and tourists. At the same time an observational study was done using the
methodology described by Gruber at al (Gruber et al, 2000), quantifying the frequency of incidence of
seven behaviour categories: aggression, comfort, ingestion, locomotion, resting, social, and stereotypy at 5
minute intervals.
Results: 6 elephants were studied over the study period. Faecal glucocorticoid metabolite (FGM)
concentrations in four elephants were not positively correlated to the number of tourist interactions per
day, the FGM concentrations declined with a 3rd
tourist interaction. One elephant’s FGM concentrations
declined with the number of interaction per day. Another elephants FGM concentrations had the highest
incline with the number of interactions per day, but had the lowest FGM concentrations of all the
elephants. Correlation with the behavioural observations found that this elephant finds interactions
positively reinforcing, thus it seems that the rise in FGM concentrations in this elephant is not a cause of
serious pathological process but rather a behavioural symptom of excitement.
Similar species-typical behavioural activities were observed in all the elephants during tourist-interactions,
while foraging or in stables. Stereotypies accounted for 0.76% of the behavioural activities and were only
seen in one elephant, just before food presentation, but whose FGM concentrations declined with each
tourist-interaction also showed the highest social behavioural activities, therefore we assumed that the
stereotypies where a behavioural symptom of anticipation and not of serious pathological process. There
were no occurrences of aggression.
Conclusion: Changes in fecal glucocorticoid metabolites were in keeping with the elephants not
experiencing stress from contact with handlers and tourists. This was supported by the behavioural
measures. Results from these also suggest that training appears to engage the animals on a cognitive level
and allows positive interaction with handlers and tourist. The welfare of these small cohort of trained
African elephants seemed not to be impaired by exposure to handlers and tourists.
Key words: Loxodonta africana, training, tourist, welfare, faecal glucocorticoid metabolites, species-typical
behaviour stress.
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Introduction
African elephant populations are present in several wildlife reserves in South Africa. Their
populations have increased to such a degree that there is concern that they are altering
vegetation (Trollope et al. 1998) and degrading ecosystems (Owen Smith. 1996; Whyte et al.
2003; Guldemond & van Aarde. 2007). Controlling the excess is possible through
contraception (Fayrer-Hosken et al. 2001), culling excess animals (van Aarde et al. 1999), or
translocation to alternative wildlife reserves. The population increase has led to a decrease in
the demand to relocate elephants. Reserves are therefore unable to find new locations for
their excess elephants, even if new owners could obtain them at no cost. After considering all
the above population control methods that are allowed by the National Norms and Standards
for the management of Elephants in South Africa (NN&S) (Biodiversity Act, Act 10. 2004),
the decision in these circumstances is often to cull the elephants.
As an alternative to this wild elephants are tamed and trained for Elephants safaris in the
tourism industry. The use of elephants in this type of tourism business offers tourists the
opportunity to have close contact with tame elephants and learn about this species.
An increasing body of research has studied elephants in these types of environments
(Wiedenmayer and Tanner, 1995, Dunlap and Scahll 1985, Wingfield and Farner 1993,
Sapolsky et al 2000). Wiedenmayer and Tanner (Wiedenmayer and Tanner, 1995) showed
that when elephants are unable to perform species-typical behaviours, such as foraging for
food, social interactions, play behaviour, and locomotion, elephants in captivity may develop
pathological behaviours known as stereotypies. It has been argued that this may result in the
manifestation of physiological issues that could compromise immune function, resistance to
disease, and survival (Dunlap and Scahll 1985, Wingfield and Farner 1993, Sapolsky et al
2000).
Elephant handlers and owners of such safari companies claim however that the elephants
used strengthen their relationship with people and remain secure and confident and at peace
in their extended human elephant community. They also state that being handled and in
contact with a large number of different people does not pose a physiological or behavioural
strain on the animals. Elephants that are present at elephant back safari operations were free
ranging elephants captured during yearly culling operations in Zimbabwe and Kruger
National Park or captured in private game reserves after escaping from state owned game
reserves. The NN&S prohibits the capture of free ranging wild elephants for the use in the
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tourism industry. An elephant may only be kept captive if it is already captive, it is captive
bred, it is from a wild population and proved that the elephant is an orphan calf (NN&S.
Biodiversity Act 10., 2004). This is, in part, due to concerns over the welfare of elephants
kept in captivity.
Animal welfare includes a set of variables such as behaviour, health, reproduction and
longevity (Laule 2003, 969). The reproductive success of captive elephants seems low when
compared to wild elephants (Moss 1988; Taylor and Poole 1998; Olson and Wiese 2000;
Wiese 2000; Rees 2003) and their longevity is not greater, even under the most favourable
conditions than that of free-ranging elephants (Wiese and Willes 2004). Captive elephants do
not have the same opportunity as free-ranging elephants, to engage in a full repertoire of
natural behaviours – occupational, social, migratory and feeding (Clubb and Mason 2002).
The majority of this research however has been carried out in elephants kept in zoos. Zoos
often keep elephants in an environment with inadequate space that is unchanging and sterile
in comparison to the wild (Laule 2003). Elephants in zoos are denied natural family groups,
which could be a reason why only few elephants in captivity are reproductively or socially
competent (Rees 2001).
Elephants in the wild possess distinct personalities, interest and histories (Moss 1988), they
live in family groups and show strong lifetime friendships (Moss 1988; Sukumare 2003).
They are cognisant and are capable of suffering both mentally and physically (Moss 1988).
As physically vigorous animals, elephants possess the stamina and strength to modify forests
into savanna and moves frequently through large areas (Poole 1997).
In the pursuit to improve the welfare of the captive populations, an environment must be
created that offers opportunities to the animal to exhibit natural behaviours (Desmond 1994).
Stress is used as a concept to at least partly encapsulate the philosophy of welfare in a
physiologically definable way. Stress however is a complex concept. It entails alterations in
behaviour as well as neuro-endocrine and autonomic function, and is reliant on the central
nervous system that assesses whether a stimulus or a group of stimuli (stressor or stressors)
exemplify a significant challenge to an organism (Seylye 1936, Burchfiled 199, O’Connor et
al. 2000, Sapolsky 2002).
The stress response is a succession of adaptive mechanisms that are designed in protecting
the organism and restoring homeostasis (Burchfield, 1979., O’Conner et al. 2000, Sapolsky
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2002, Bomholt et al. 2004) The outcome of a stressor can be monitored by measuring
physiological responses or by quantifying behavioural responses, though this tends to be
more subjective (Pretorius 2004, Weary et al. 2006).
A free-ranging animal is in a state of stress if it is obligated to make abnormal or radical
adjustments in its physiology or behaviour so as to cope with adverse facets of its
environment or management (Friend 1980). From the physiological standpoint, a number of
endocrine responses are involved during stress situations. Some of the frontline hormones
produced in these situations are the glucocorticoids, which are indicators of adrenocortical
activity and thus are elevated in times of stress (Möstl & Palme 2002).
In the course of courtship, copulation or predatory behaviour, circulation glucocorticoid (GC)
can improve fitness by activating energy or mediating physiological and behavioural
modifications, although on a temporary basis (Möstl & Palme 2002, Touma & Palme 2005).
Nevertheless, chronic stress can have negative consequences on health since the related
prolonged periods of elevated GC levels may reduce fitness by causing immunosuppression
and atrophy of tissues (Munck et al. 1984, Möstl & Palme 2002). Furthermore, the episode
of stress is also well known to have disruptive effects for instance on reproduction, cognition
and behaviour in vertebrates (Liptrap 1993, Möstl & Palme 2002, Sapolsky 2002) In this
regard, the investigation of glucocorticoids can be a helpful tool for studies in animal
welfare in captivity.
Collecting blood or saliva samples are disagreeable to the elephants and the stress associated
with handling during collection can elevate recorded cortisol concentrations, invalidating the
data. It is therefore favourable to measure cortisol non-invasively and to use a method that
provides samples more representative of current concentrations (Lane, 2006). The advantage
of Faecal samples is that it can easily be collected, and Stead et al (2000), Wasser et al
(2000), Foley et al. (2001) and Ganswindt et al (2003, 2005) have developed non-invasive
methods and successfully tested it to enable the measurement of glucocorticoid metabolites in
elephant faeces.
It is viable to describe behaviours that may be symptomatic of the presence or absence of
stress (Garaĭ.1997). There is growing evidence that emotional and physical stress can cause
behavioural and physiological alterations in an animal. The intense concern of, or violent
behaviour towards, humans, sometimes recorded in elephants (Garaï et al. 2004), may be
both instigate and outcome of negative stressful events and can cause safety problems for
6
both elephants and humans in the elephant back safari industry. ). Events such as being faced
with peril, an adversary or lack of food result in behaviour patterns that are coupled with the
autonomic nervous system, thus fight-flight responses are common (Toates. 1995). Such
responses should not be of concern because they fall within the natural adaptive range of the
animal. Nevertheless, problems may occur when conditions avoid the animal from expressing
behaviours in response to stressors or when behaviours, such as foraging and grooming,
cannot be performed (Wiepkema et al. 1993). Such circumstances are usually found in
captive conditions and often result in chronic stress responses, seen as stereotypic or injurious
behaviour. These responses are characterised by the truth that the incidence of permanent
stressors or one or two encounters with a drastic stressor have a long lasting after effect
(Wiepkema et al. 1993). Chronic stress is often expressed when animals cannot predict and/
or control relevant events in their environment (Weiss. 1972). Abnormal behaviours,
especially stereotypies, are frequently used as indicators of welfare.
Stereotypies can be defined as unvarying, persistent behaviours that have no obvious goal or
function (Fox, 1965; Hutt and Hutt, 1965). Stereotypes have been coupled with sub-optimal
housing or management systems (Mason, 1991) and are thought to develop due to the
inability of captive animals to choose a desired behaviour (Mason, 1991) or be in charge of
their environment (Carlstead, 1996). They are not carried out in the wild, thus unusual
behaviour. Stereotypies may be instigated by a large number of factors, but often develop
from early attempts at escape and portray a ritualised form of this behaviour (Cronin et al.
1986).They may indicate fear (Mason. 1991), inescapable lack of control (Weiss. 1972), lack
of natural social contacts (Berckson. 1963) or the absence of investigative behaviour (Bryant
et al. 1989). They normally become facilitated by daily routines in captive conditions
(Rushen. 1995). It has been recommended that in stressful conditions, stereotypy is a coping
response consequential in a reduction of hormonal response to stress (Mason. 1991). Mason
and Latham (2004) proposed that most (approximately 68%) situations that cause or increase
stereotypies also decrease welfare. Stereotypy-educing situations are thus likely to be poor
for welfare, although exceptions exist. There are four processes that could link stereotypies to
welfare but, stereotypies should never be used as a sole indicator for welfare (Mason &
Latham, 2004)
The present study is a pilot study to explore the hypothesis that the environment offered by a
tourist-aimed elephant back safari park may be one which provides the elephant’s needs. To
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test this hypothesis both physiological i.e. glucocorticoid and observational i.e. behavioural
measures of stress were used.
Material and Methods
The study design is based on the two questions proposed by Dawkins (2008):
Q1: “Are the animals healthy?”
Q2: “Do the animals have what they want, as defined by what they find positively
reinforcing?”
Validated outcome measures were used, that is on measures of behaviour and physiology of
the elephants, to test these questions (Broom & Johnston 1993; Appleby & Hughes 1997;
Wechler 2007).
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1. Materials: the elephants
Six tamed and trained African elephants aged 9 – 26 years were the subject of the study. Data
collection entailed observing each elephant’s behaviour and the collection of faecal samples.
Details of each African elephant are presented in Table 1.
Table 1: Six elephants from the elephant safari company.
Elepha
nt
S
e
x
A
g
e
Captur
ed
N
u
m
be
r
of
tr
an
sl
oc
ati
on
s
M
on
th
s
at
EF
AF
M
oo
ke
tsi
Arrive
d at
Eleph
ant
Whis
pers
Boma
size (m²)
Level of
tourist
human
contact
Thembo M 27 03/11/27 3 30 08/04/29
42m²
High level of
contact
Ziziphus M 15 06/04/17 3 17 08/04/29
84 m²
Moderate level
of contact
Medwa M 15 06/04/17 2 20 07/12/05
42 m²
High level of
contact
Shimwari M 15 05/07/13 2 29 07/12/05
42 m²
Moderate
level of contact
Lindiwe F 10 06/04/17 2 20 07/12/05
42 m²
High level of
contact
Andile F 14 07/03/08 2 23 09/04/16
42 m²
Moderate level
of contact
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Table 2: Elephant-tourist interactions.
Excursion Duration Times Description
Elephant
interaction
1 hr 09:00
12:00
16:00
• Brief history of each elephant.
• Demonstrating how elephants are trained
• Medwa interaction: interpretation on elephants, clients
allowed to offer treats and take pictures, touch Medwa while
he’s laying down
• Thembo interaction: interpretation on elephants, clients stand
between his legs for a picture.
• Lindiwe interaction: interpretation on elephants, clients are
asked to give Lindiwe commands and to reward her with a
treat when she responds correctly.
Interaction and
ride
1 hr 30 min 09:00
12:00
16:00
• Interaction as described above
• Ride: 2 people on each elephant, 20 min long
Ultimate
Interaction and
ride
2 hr 30 min 12:00 • Interaction and ride as described above
• Elephants bath in water hole; clients enjoy lunch on deck
watching.
Early morning
wake up, and
elephant back ride.
2hr 06:30 • Clients are taken to the Stables
• Grooms open stables of elephants
• Clients are allowed to brush elephants down
• Interaction and ride as described above
Sunset interaction,
elephant back ride
2hr 16:00 • Interaction and ride as described above
• Clients are taken to the Stables
* Treats and barna grass are offered to the elephants during interactions.
All the elephants received an examination by a veterinary surgeon to confirm that they were
in good physical health.
2. Methods:
The aim of this study was to assess a correlation between human handling and the occurrence
of stereotypical behaviours and potential changes in adrenocortical activity in six trained
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African elephants used by an elephant safari company in South Africa. Two studies were
done over a period of one year. Both Physiological and behavioural outcomes were
measured, since periodicity of cortisol release and other hormones which interact and affect
the adrenocortical system may influence findings (Dawkins. 1980).
2.1 Glucocorticoid sampling and measuring:
The enzyme immunoassay (EIA) technique was used to measure the faecal glucocorticoid
metabolites in the elephants according to the procedure described by Viljoen et al (2008) and
Ganswindt et al (2005 b).
Faecal samples were collected as soon as possible after defecation from the individual
elephants. One sample from the six elephants was collected during any of the interaction
excursions at 09h00, 12h00 or 14h00. Rubber gloves was used to collect roughly 100 grams
of homogenous faecal material from the middle of the bolus to avoid cross-contamination
with urine or other faecal samples and then placed in a labelled glass container with an air
tide lid. All faecal samples were frozen within 2 hrs of collection and stored at -8 °C until
analysis at the Endocrine Research Laboratory of the University of Pretoria. Each sample was
marked with the date of collection, time of collection, and the name of the elephant. Faecal
samples was collected once a week over demanding and subtle tourism phases, which
allowed us to determine, through concentrations of immunoreactive glucocorticoid
metabolites, whether the interaction activities with tourist have any possible disruptive
influence on an elephant’s normal physiological stability. Samples were collected from
December 2009 until September 2010. At the end of each month an outline of the tourist-
elephant interaction excursions were documented.
Faecal samples were lyophilized, pulverized, and sieved through a mesh to remove
undigested faecal matter as described by Fieß et al (1999). An approximate 0.05 g of the
faecal powder was then extracted by vortexing for 15 min with 80% methanol in water (3
mL). Following centrifugation for 10 min at 3,300g, supernatants was transferred to a glass
tube and then ready for hormone analysis. Faecal extracts were measured for immunoreactive
glucocorticoid metabolites using an enzyme immunoassay for 3α, 11oxo-cortisol metabolites
(3α,11oxo-CM) (Möstl et al. 2002), which has previously been shown to provide reliable
information on adrenocortical function in the African elephant (Ganswindt et al 2003, 2005).
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2.2 Behavioural study:
The observer performed observations during interaction excursions once a week for each
elephant (see Table 1) which were recorded on a prepared check sheet (Appendix 1) based on
the ethogram drafted by Gruber et al (2000). The instantaneous scan sampling technique
(Altmann, 1974 & Martin and Bateson, 1993) was used at 5 minute intervals. All behaviour
identified was allocated to one of the seven activity states. These are aggression, comfort,
ingestion, locomotion, resting, social and stereotypies (Gruber et al. 2000). To identify
behaviour that was thought to be normal behavioural studies were conducted while the
elephants were foraging as well as while they were in the stables. The same types of
behaviour were recorded as with the interactions.
3. Results:
3.1. Glucocorticoid analysis:
A number of variables were considered and models were fitted to determine the relationships
between variables and faecal cortisol levels. A number of elephant related variables were
considered being Animal, Age, Sex, Dominance ranking, and length of training.
When models were run using these variables many were auto correlated and the animal name
was retained in the model. Variables considered determining whether interactions are
affecting GCM values were no of people taking part in the interaction this was classed to be
small groups which consisted of groups less than 30 people and large groups > 30 people. Nr
of Interactions and nr of Rides in the 25 hours period before the GCM sample was taken were
also recoded as well as the number of interactions that had less than 2 hours in between
interactions as the assumption here was that if the foraging time between Elephants was
reduced that they could be more stressed. Environmental variables considered were Rainfall
and Month of year.
A 164 (mean 27 samples per individual) faecal samples were collected between December
2009 and September 2010 and FGM concentrations were successfully obtained.
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Linear regression models were used to predict the relationships between faecal cortisol levels
and the variables mentioned above. When fitting these models the constant error variance
assumption was violated a small p value was obtained and there was an indication of
clumping in the centre as well as funnelling at larger values. To correct for this Generalise
Least Square (GLS) approaches were used. GLS assumes a different relationship between the
residual variance and the fitted values.
Figure 1: Median GCM levels for the 6 different Elephants
There was no correlation between age and FGM concentrations, as discovered by Munshi-
South et al (2008) where adults have significantly higher FGM concentrations than juveniles.
Dominance ranking were not correlated with FGM levels as previously revealed by
Ganswindt et al (2005), where FGM concentrations during periods of aggressiveness were
significantly lower than those of animals in a nonaggressive condition.
The concentrations of FGM in the six African elephants were not influenced by seasonal
changes. There was no elevation of concentrations of FGM during the dry season as
Andile Lindiwe Medwa Shimwari Thembo Zizi
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previously discovered by authors (Foley et al 2001; Ganswindt et al. 2005; Rasmussen et al.
2008, Viljoen et al. 2008b, Ganswindt et al. 2010). This could be due to the high quantity and
nutritional value of food provided to the elephants. Codron et al (2006) stated that the
percentage of nitrogen in elephant faeces from the southern KNP showed a significant
increase from the dry to the wet season. An elevation of nitrogen in faeces is known as a
useful indicator of nutristional status.
There was no significant correlation between FGM levels and the sex of the elephant; but
Andile’s FGM concentration profile tend to have a inclination towards a cycling female
elephants progestogen profile (Brown, 2000). Foley et al (2001) established that cortisol
metabolite and progesterone concentration are significantly correlated. However, this is not
conclusive and progesterone and FGM values needs to be assessed simultaneously, through
weekly collection of faecal samples
The number of rides became significant at the 10% level. When one looks at interaction plots
below the first one showing the Elephant name, GCM value and the Nr of Rides, one can
clearly see that there is a significant variation in the cortisol values between the elephants.
Andile has the highest GCM value all the time and the effects that one may expect to see
could, with the different number of rides, be reduced because of the inter elephant variation.
One needs then to compare each elephant to itself and unfortunately the amount of data will
not allow us to do this. For example Lindiwe, who has the lowest cortisol value, has the
biggest effect when a second ride is added.
14
15
A similar effect was apparent when the number of interactions was analysed. Andile, once
again has the highest levels. Lindiwe the lowest and there is quite a marked increase in
Lindiwe compared to the others. It therefore appears that the individual elephant itself has the
greatest effect on the cortisol levels and if one would like to start looking at different
interaction group and ride sizes one may want to only look at the highest and lowest elephant
and get a large samples size for these.
How each elephant respond to the interactions and rides can be reflected in their mean FGM
concentrations, each elephant are different from another elephant.
The rise in FGM concentration and the number of interactions:
Elephant Mean FGM concentration from 1 to 2
interactions
Mean FGM concentration from 2 to 3
interactions
Lindiwe Increases 1,26 fold Increases 1,03 fold
Shimwari Decreases 0,99 fold Decreases 0,9 fold
Medwa Increases 1,17 fold Decreases 0,83 fold
Thembo Increases 1,29 fold Decreases 0,84 fold
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Andile Increases 1 fold Decreases 0,89 fold
Ziziphus Increases 1,03 fold Increases 1,01 fold
The rise of FGM concentrations correlates with the number of rides
Elephant FGM concentration when
more than 1 ride
Lindiwe Increases 1,24 fold
Shimwari Decreases 0,98 fold
Medwa Increases 1,03 fold
Thembo Increases 1,06 fold
Lindiwe Increases 1,06 fold
Ziziphus Increases 1,05 fold
Taken as a whole, FGM concentrations increased 1, 12 fold when a second interaction
occurred. When a third interaction occurred FGM concentrations in Lindiwe and Zizi
increased 1, 02 fold more, but decreased 0, 87 fold in the other 4 elephants. Lindiwe’s shows
a more significant respond to interactions, but she has the lowest mean FGM concentrations..
FGM levels increased 1, 09 fold when more than one ride occurred, but FGM levels in
Shimwari decreased 1, 09 fold. Again Lindiwe is showing higher response, but still has the
lowest mean FGM concentrations. The number of interactions and rides seems not to have a
significant correlation with mean FGM concentrations in elephant. Each elephant has a
unique FGM.
Behavioural analysis:
The observational data was lumped across all the Elephants since the number of observations
taken from the three different activities were not equal. Proportions were calculated for each
type of behaviour and these were then totalled over the different categories above to get one
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proportion per category. A student t test was then used to calculate whether there were
significant differences between the observations observed in the different activities.
Between-observer reliability was measured to determine the accuracy of behaviour
definitions used within each category. An interaction excursion was randomly selected and
the two observers independently measured each elephant’s behaviour at 5-minute intervals
for the entire excursion using the Gruber’s et al ethogram (Table 1). An index of
concordance, comparing the total number of agreements (A) and disagreements (D), were
performed using the formula I = A/ (A+D) (Martin and Bateson, 1993). Within-observer
reliability was measured to determine whether there is any “observer drift” during the
duration of the study. An interaction excursion was selected at random, and on two separate
occasions the same observer measured each elephant’s behaviour at 5-minute intervals using
the Gruber’s et al ethogram (Table 3). An index of concordance was then be performed using
the formula I = A/ (A + D) (Martin and Bateson, 1993).
The results from both studies were compared. evaluated with baseline concentration of faecal
glucocorticoid metabolites in captive and free-ranging African elephants (e.g Ganswindt et al
2003; 2005a; b; 2009; Viljoen et al., 2008 a; b) and against known behavioural indicators of
stereotypies in captive elephants identified by Garaĭ (1997) and Gruber et al (2000).
Physical variables: geographic range and body size.
The six trained African elephants are kept in a 4000 hectare conservancy located in the
Lowveld’s savanna, which is analogous to geography of the Kruger National Park.
Husbandry of the six elephants is currently under the supervision of the Department of
Environmental Affairs and Tourism (DEAT).
The boma layout consists of seven 42m² stables and one 84m² stable for Thembo (3m in
shoulder height) and is assembled with 4m gum poles 200mm diameter thick under a
corrugated roof. The design is open, well ventilated and allows the elephants to release excess
heat into the atmosphere they store above 23 C as Langman advices (1990). The elephants
also have complete visual and tactile contact amongst each other, as articulated by Clubb &
Mason (2002).
18
The floor of each stable is rounded to allow adequate runoff into a furrow and is often treated
with an organic insecticide. The top layer of the floor is regularly removed and replaced with
new soil.
The elephants enter the stables at 17:30 and are provided with bedding and fresh cut branches
from indigenous trees at 18:00 and 24:00 and let out at 07:00. Fresh drinking water is kept in
a reservoir outside the stables. The elephants are able to drink and splash themselves with
water before they go into the stables in the evening and in the morning before starting their
day. Water was kept in their stables, but the elephants played more with it than drinking it
which created mud pools in their stables. Cleaning of stables starts soon after the elephants
have left their stables, the dung is moved to a compost heap and the left over branches are
first deposited into a chipper and then thrown onto the compost heap, to decrease exposure to
potentially dangerous compounds from faeces and urine (Veasey, 2006). After their morning
training and exercise session, the elephants are allowed to roam free in the 4000 hectare
conservancy, while watched over by four grooms. The elephants are brought together at the
interaction site when there is a tourist interaction.
The six elephants are able to shed excess body heat between interactions in the rivers and
waterholes, and during interactions, if they require it, can be drenched with hose water. The
exhibit and conservancy provide elephants with environmental options that allow them to
regulate their body temperature effectively as recommended by Langman’s (1990, 1996,
2003) and Rees’s (2002) research.
The stables are in proximity to a public road, and there are sometimes large trucks driving
past.
Occupational variables: activity cycle and habitat use.
19
There is a specific activity routine set out for the elephant’s everyday. The day start 07:00,
the elephants are let out of the stables and move towards the reservoir for a drink and a splash
of water. Before free ranging, a 20 minute exercise activity is conducted. Depending on the
bookings, tourist interactions are at 09:00, 12:00 and 16:00, which last approximately 2 hours
each (sometimes only one or two interaction is done per day). Elephants free range between
interactions. Elephant are taken back to stables at 18:00, and allowed to drink and splash
water, and immediately provided with fresh cut browse, which is in small piles outside the
stables, they are again fed at 21:00 and 24:00. The activity sketch of these elephants is
polycyclic.
The elephants occupy more or less 18 hours of their day browsing or grazing. They are in
motion almost continuously while feeding. The rest of their day is mostly given over to
socializing, water or dust bathing, or wallowing in mud. They rest for about 4 hours a day,
either in a recumbent or in standing position only in their stables. This occupational pattern is
analogous to their cohorts in the wild (Moss, 1988; Eisenberg 1981).
There are many options accessible to the six captive elephants permitting them to maintain a
natural activity pattern. The habitat of the conservancy can be described as dense bush on the
uplands, open tree savanna in the bottomlands with waterholes and mud pools, and dense
riverine woodland on the river. It is 4000 hectares, greater than suggested by Hutchins
(2006) necessary for elephants in captivity. Options to the elephants include space to roam on
a variety of substrates, with a variation in topography, and access to suitable plant material or
substantial and free provision of cut fresh browse (branches) for species specific foraging.
They have daily access to water and mud of adequate volume to allow totally submerged
bathing and all-body wallowing.
A total of 135 observations were performed with an average length of 30 minutes between
January and September 2010.
Two students t tests were conducted the first one to determine whether there was a significant
difference in the behaviour recorded during the interactions and while the Elephants Foraged
and the second one was between the Interactions and when they were in the stables. Both of
these tests showed that there are no significant differences in behaviour.
The graph shows the different proportions that were recorded in each different behaviour
category
20
0
10
20
30
40
50
60
Aggression comfort ingestion locomotion resting social stereotypies
forage
interactions
stables
Fig. 4. The effect of forage, interactions and stables on behaviour.
The percentage of observation performing each activity was determined for each
elephant during interaction.
0
10
20
30
40
50
60
aggression comfort ingestion locomotion resting social stereotypies
medwa
lindiwe
shimwari
andile
thembo
Zizi
Discussion
This study has demonstrated, we believe for the first time, that FGM concentrations in
captive elephants exposed to daily tourist activities fall within the ‘normal’ range previously
Behavior
%
%
Behavior
21
recorded for African elephants living in the wild. Around the Samburu and Buffalo Springs
National Reserves, Kenya, 64 individual bulls showed FGM concentrations from 0.2 GCM
(µg/gDW) to 2 GCM (µg/gDW) (Fig. 2 in Ganswindt et al., 2005). In the present study it
appears that the number of interactions or rides do not demonstrate a significant physiological
challenge to the elephants. Elephants can acclimate to disturbed/ unnatural environments, as
found by Munshi-South et al (2008), where they found the African elephants in Loango
National Park exhibited significantly higher FGM concentrations than elephants in a
industrial corridor dominated by oil fields.
As previously observed by other authors, usually only severe stressors are found to have
significant effects on cortisol concentrations similar to those measured after ACTH
administrations (4 -5 fold increase; Ganswindt et al., 2003). Mean FGM concentrations
associated with translocation increased 6-7 fold (Viljoen et al. 2008a, Millpaugh et al. 2007)
and with episodic loud noices increased 3 – 4 fold. FGM concentrations in 2 physically
injured free-ranging African elephants increased 3 fold (Fig. 2 in Ganswindt et al., 2010).
Seasonal variance in FGM concentrations of African elephants increased more than 2 fold
between regular seasons (Foley et al. 2001, Viljoen et al. 2008b).
Glucocorticoids (GC’s) are a classic endocrine response to stress. Despite that, it remains
litigious as to what purpose GC’s serve at such times. The tendency to think that the stress
axis is only a response of the body to short-term stressors is wrong, since it also plays a key
role to carry out the daily functions of living (McEwen 2001). It is associated with the diurnal
cycle of waking such as increased locomotion, increased appetite, exploratory behaviour and
food-seeking behaviour (reviewed by McEwen et al, [1998], Reeder & Kramer [2005], and
Wingfield & Romero [2001]. Dallman and colleagues found that glucocorticoid
concentration has a pronounced circadian rhythm, being highest at the onset of daily activity
and lowest at the end of it.
Behaviourally the elephants spent more time in comfort, ingestion and locomotion activities
than in social and resting activities. Stereotypies barely occurred and there were no
occurrences of aggression. Stereotypic behaviours are generally considered as indicators of
poor welfare (Kiley – Worthington 1990; Gruber et al 2000). Gruber et al (2000) studied the
effect of penning and chaining on circus elephants and found stereotypies accounted for 20 -
45 % of the behaviours. Similar behaviour was found in other studies. In Sri Lanka, weaving
in circus elephants, were whenever they had to wait for something or where expecting
22
something. They increased the frequencies of weaving before they were fed or when they
were expecting water. Elephants observed during the Kandy Perahera weaved before they
were fed (Kurt & Garai, 2001). Stereotypic behaviours help the animal cope with unpleasant
stimulation or boredom and animals performing these behaviours therefore have lower heart
rates and reduced cortisol levels than not-stereotypic animals under the same conditions
(Clubb & Mason, 2002; Veasey, 2006).
They engaged in a full range of natural behaviours also seen in wild elephants (Clubb and
Mason 2002). Their mean faecal glucocorticoid metabolite concentrations were similar to
wild elephants, except that their mean FGM levels do not elevated during the dry season as
found in wild elephants (Foley et al. 2001; Rasmussen et al 2008; Viljoen et al. 2008b;
Ganswindt et al 2010).
The elephants did not exhibit behaviours of aggressive or stereotypies as seen in elephants
under stress (Garai, 1997; Hutchins, 2006, Clubb & Mason, 2002).
It also appears that the elephants experience human handling positively, since they continue
to do the activities willingly. Olson substantiates: “behaviour does not occur as isolated and
unrelated events; the consequences that follow the actions of an elephant, whether good, bad,
or indifferent, will have an effect upon the frequency which those actions are repeated in the
future.” “All reinforcement increases the likelihood of a behaviour being repeated.” The
positive reinforcers seem to be the combination of getting attention, being praised and getting
a reward. The elephants seem to have control over their own behaviour. This is exceptionally
important since research on stress specifies that the ability to exercise control over an
environment, even if the stress stimulus cannot be removed, exceedingly lowers the degree of
stress experienced by the animal (Seligman et al. 1977; Foster-Turley et al 1982; Markowitz
et al 1989; and Laule and Desmond 1998).
1. Conclusion
This paper, for the first time, suggests that the hypothesis that wild elephants trained and kept
in back-safari tourist parks do not experience undue stress from the experience. It is
important however to highlight the large size of the park and the focus on the welfare of the
elephants demonstrated by the park staff.
23
The study results support the following recommendations to establishments managing trained
elephants in close contact with tourist:
1) the elephants must occupy a large enough habitat providing conditions promoting species-
appropriate behaviour as revealed by this species’ natural history (Mench and Kreger 1996,
Hancocks 1996; Coe 2003).
2) Herd mates must be compatible, which is a highly effective form of enrichment and
therefore important (Hutchins, 2006; Veasey, 2006).
3) The elephants must not experience any unnecessary pain or distress.
4) A training regime predicted on positive reinforcement and respect for the animal’s
autonomy is best suited to enhance the lives of the elephants and providing for their
psychological well-being.
5) A routine activity pattern so that the elephants can learn what to expect next. Elephants
will have a sense of control over their environment and are required to make less abnormal or
extreme adjustments in their physiology or behaviour. (Friend, 1980; Carlstead, 1996;
Mason, 1991).
6) Elephants must be able to partake in species-typical behaviours, even when they are
interacting with tourist or when they are in stables.
7) Monitoring the faecal glucocorticoid metabolite in conjunction with behavioural
observation is a useful diagnostic tool to understand how elephants respond to training and
interacting in close contact with humans.
Acknowledgements
Special thanks to Andre Kotze, who supervises the care and guidance of these elephants, and
the elephant handlers at Elephant Whispers, for their support and assistance. The author
thanks Rory and Lindi Hensman from Elephants for Africa forever, for their background
information on these elephants. The author is grateful to Dr Andre Ganswindt for providing
access to the reagents of FGM enzyme immunoassays and Stephany Münscher for expert
help in laboratory techniques. The author is also grateful to Judith Botha, Dr. Andre
Ganswindt and Dr. Anje J Higgo for reviewing the manuscript, with special thanks to Judith
24
Botha for the statistical analysis. The study was funded in part by Elephant Whispers and the
University of South Africa.
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Marina's thesis v1

  • 1. 1 The physiological and behavioural effect of human handling on trained African elephants (Loxodonta africana) Marina Visser
  • 2. 2 ABSTRACT: Introduction: Domesticated African elephants (Loxodonta africana) are used for elephant-back safaris and interactions with tourist. The keeping of elephants is currently under debate, since they are highly intelligent and social animals (Veasey, 2006). Measuring the welfare of these elephants is critical since it can have serious consequences such as reproductive problems, occurrence of stereotypic behaviour, higher incidences of aggression and diseases and a higher death rate. Methods: Faecal glucocorticoid metabolites were analyzed using a validated enzyme immunoassay (Ganswindt et al, 2003) to assess physiological stress in a sample of trained African elephants at an elephant-back safari company. These elephants were experiencing daily exposure to and handling by humans both trained handlers and tourists. At the same time an observational study was done using the methodology described by Gruber at al (Gruber et al, 2000), quantifying the frequency of incidence of seven behaviour categories: aggression, comfort, ingestion, locomotion, resting, social, and stereotypy at 5 minute intervals. Results: 6 elephants were studied over the study period. Faecal glucocorticoid metabolite (FGM) concentrations in four elephants were not positively correlated to the number of tourist interactions per day, the FGM concentrations declined with a 3rd tourist interaction. One elephant’s FGM concentrations declined with the number of interaction per day. Another elephants FGM concentrations had the highest incline with the number of interactions per day, but had the lowest FGM concentrations of all the elephants. Correlation with the behavioural observations found that this elephant finds interactions positively reinforcing, thus it seems that the rise in FGM concentrations in this elephant is not a cause of serious pathological process but rather a behavioural symptom of excitement. Similar species-typical behavioural activities were observed in all the elephants during tourist-interactions, while foraging or in stables. Stereotypies accounted for 0.76% of the behavioural activities and were only seen in one elephant, just before food presentation, but whose FGM concentrations declined with each tourist-interaction also showed the highest social behavioural activities, therefore we assumed that the stereotypies where a behavioural symptom of anticipation and not of serious pathological process. There were no occurrences of aggression. Conclusion: Changes in fecal glucocorticoid metabolites were in keeping with the elephants not experiencing stress from contact with handlers and tourists. This was supported by the behavioural measures. Results from these also suggest that training appears to engage the animals on a cognitive level and allows positive interaction with handlers and tourist. The welfare of these small cohort of trained African elephants seemed not to be impaired by exposure to handlers and tourists. Key words: Loxodonta africana, training, tourist, welfare, faecal glucocorticoid metabolites, species-typical behaviour stress.
  • 3. 3 Introduction African elephant populations are present in several wildlife reserves in South Africa. Their populations have increased to such a degree that there is concern that they are altering vegetation (Trollope et al. 1998) and degrading ecosystems (Owen Smith. 1996; Whyte et al. 2003; Guldemond & van Aarde. 2007). Controlling the excess is possible through contraception (Fayrer-Hosken et al. 2001), culling excess animals (van Aarde et al. 1999), or translocation to alternative wildlife reserves. The population increase has led to a decrease in the demand to relocate elephants. Reserves are therefore unable to find new locations for their excess elephants, even if new owners could obtain them at no cost. After considering all the above population control methods that are allowed by the National Norms and Standards for the management of Elephants in South Africa (NN&S) (Biodiversity Act, Act 10. 2004), the decision in these circumstances is often to cull the elephants. As an alternative to this wild elephants are tamed and trained for Elephants safaris in the tourism industry. The use of elephants in this type of tourism business offers tourists the opportunity to have close contact with tame elephants and learn about this species. An increasing body of research has studied elephants in these types of environments (Wiedenmayer and Tanner, 1995, Dunlap and Scahll 1985, Wingfield and Farner 1993, Sapolsky et al 2000). Wiedenmayer and Tanner (Wiedenmayer and Tanner, 1995) showed that when elephants are unable to perform species-typical behaviours, such as foraging for food, social interactions, play behaviour, and locomotion, elephants in captivity may develop pathological behaviours known as stereotypies. It has been argued that this may result in the manifestation of physiological issues that could compromise immune function, resistance to disease, and survival (Dunlap and Scahll 1985, Wingfield and Farner 1993, Sapolsky et al 2000). Elephant handlers and owners of such safari companies claim however that the elephants used strengthen their relationship with people and remain secure and confident and at peace in their extended human elephant community. They also state that being handled and in contact with a large number of different people does not pose a physiological or behavioural strain on the animals. Elephants that are present at elephant back safari operations were free ranging elephants captured during yearly culling operations in Zimbabwe and Kruger National Park or captured in private game reserves after escaping from state owned game reserves. The NN&S prohibits the capture of free ranging wild elephants for the use in the
  • 4. 4 tourism industry. An elephant may only be kept captive if it is already captive, it is captive bred, it is from a wild population and proved that the elephant is an orphan calf (NN&S. Biodiversity Act 10., 2004). This is, in part, due to concerns over the welfare of elephants kept in captivity. Animal welfare includes a set of variables such as behaviour, health, reproduction and longevity (Laule 2003, 969). The reproductive success of captive elephants seems low when compared to wild elephants (Moss 1988; Taylor and Poole 1998; Olson and Wiese 2000; Wiese 2000; Rees 2003) and their longevity is not greater, even under the most favourable conditions than that of free-ranging elephants (Wiese and Willes 2004). Captive elephants do not have the same opportunity as free-ranging elephants, to engage in a full repertoire of natural behaviours – occupational, social, migratory and feeding (Clubb and Mason 2002). The majority of this research however has been carried out in elephants kept in zoos. Zoos often keep elephants in an environment with inadequate space that is unchanging and sterile in comparison to the wild (Laule 2003). Elephants in zoos are denied natural family groups, which could be a reason why only few elephants in captivity are reproductively or socially competent (Rees 2001). Elephants in the wild possess distinct personalities, interest and histories (Moss 1988), they live in family groups and show strong lifetime friendships (Moss 1988; Sukumare 2003). They are cognisant and are capable of suffering both mentally and physically (Moss 1988). As physically vigorous animals, elephants possess the stamina and strength to modify forests into savanna and moves frequently through large areas (Poole 1997). In the pursuit to improve the welfare of the captive populations, an environment must be created that offers opportunities to the animal to exhibit natural behaviours (Desmond 1994). Stress is used as a concept to at least partly encapsulate the philosophy of welfare in a physiologically definable way. Stress however is a complex concept. It entails alterations in behaviour as well as neuro-endocrine and autonomic function, and is reliant on the central nervous system that assesses whether a stimulus or a group of stimuli (stressor or stressors) exemplify a significant challenge to an organism (Seylye 1936, Burchfiled 199, O’Connor et al. 2000, Sapolsky 2002). The stress response is a succession of adaptive mechanisms that are designed in protecting the organism and restoring homeostasis (Burchfield, 1979., O’Conner et al. 2000, Sapolsky
  • 5. 5 2002, Bomholt et al. 2004) The outcome of a stressor can be monitored by measuring physiological responses or by quantifying behavioural responses, though this tends to be more subjective (Pretorius 2004, Weary et al. 2006). A free-ranging animal is in a state of stress if it is obligated to make abnormal or radical adjustments in its physiology or behaviour so as to cope with adverse facets of its environment or management (Friend 1980). From the physiological standpoint, a number of endocrine responses are involved during stress situations. Some of the frontline hormones produced in these situations are the glucocorticoids, which are indicators of adrenocortical activity and thus are elevated in times of stress (Möstl & Palme 2002). In the course of courtship, copulation or predatory behaviour, circulation glucocorticoid (GC) can improve fitness by activating energy or mediating physiological and behavioural modifications, although on a temporary basis (Möstl & Palme 2002, Touma & Palme 2005). Nevertheless, chronic stress can have negative consequences on health since the related prolonged periods of elevated GC levels may reduce fitness by causing immunosuppression and atrophy of tissues (Munck et al. 1984, Möstl & Palme 2002). Furthermore, the episode of stress is also well known to have disruptive effects for instance on reproduction, cognition and behaviour in vertebrates (Liptrap 1993, Möstl & Palme 2002, Sapolsky 2002) In this regard, the investigation of glucocorticoids can be a helpful tool for studies in animal welfare in captivity. Collecting blood or saliva samples are disagreeable to the elephants and the stress associated with handling during collection can elevate recorded cortisol concentrations, invalidating the data. It is therefore favourable to measure cortisol non-invasively and to use a method that provides samples more representative of current concentrations (Lane, 2006). The advantage of Faecal samples is that it can easily be collected, and Stead et al (2000), Wasser et al (2000), Foley et al. (2001) and Ganswindt et al (2003, 2005) have developed non-invasive methods and successfully tested it to enable the measurement of glucocorticoid metabolites in elephant faeces. It is viable to describe behaviours that may be symptomatic of the presence or absence of stress (Garaĭ.1997). There is growing evidence that emotional and physical stress can cause behavioural and physiological alterations in an animal. The intense concern of, or violent behaviour towards, humans, sometimes recorded in elephants (Garaï et al. 2004), may be both instigate and outcome of negative stressful events and can cause safety problems for
  • 6. 6 both elephants and humans in the elephant back safari industry. ). Events such as being faced with peril, an adversary or lack of food result in behaviour patterns that are coupled with the autonomic nervous system, thus fight-flight responses are common (Toates. 1995). Such responses should not be of concern because they fall within the natural adaptive range of the animal. Nevertheless, problems may occur when conditions avoid the animal from expressing behaviours in response to stressors or when behaviours, such as foraging and grooming, cannot be performed (Wiepkema et al. 1993). Such circumstances are usually found in captive conditions and often result in chronic stress responses, seen as stereotypic or injurious behaviour. These responses are characterised by the truth that the incidence of permanent stressors or one or two encounters with a drastic stressor have a long lasting after effect (Wiepkema et al. 1993). Chronic stress is often expressed when animals cannot predict and/ or control relevant events in their environment (Weiss. 1972). Abnormal behaviours, especially stereotypies, are frequently used as indicators of welfare. Stereotypies can be defined as unvarying, persistent behaviours that have no obvious goal or function (Fox, 1965; Hutt and Hutt, 1965). Stereotypes have been coupled with sub-optimal housing or management systems (Mason, 1991) and are thought to develop due to the inability of captive animals to choose a desired behaviour (Mason, 1991) or be in charge of their environment (Carlstead, 1996). They are not carried out in the wild, thus unusual behaviour. Stereotypies may be instigated by a large number of factors, but often develop from early attempts at escape and portray a ritualised form of this behaviour (Cronin et al. 1986).They may indicate fear (Mason. 1991), inescapable lack of control (Weiss. 1972), lack of natural social contacts (Berckson. 1963) or the absence of investigative behaviour (Bryant et al. 1989). They normally become facilitated by daily routines in captive conditions (Rushen. 1995). It has been recommended that in stressful conditions, stereotypy is a coping response consequential in a reduction of hormonal response to stress (Mason. 1991). Mason and Latham (2004) proposed that most (approximately 68%) situations that cause or increase stereotypies also decrease welfare. Stereotypy-educing situations are thus likely to be poor for welfare, although exceptions exist. There are four processes that could link stereotypies to welfare but, stereotypies should never be used as a sole indicator for welfare (Mason & Latham, 2004) The present study is a pilot study to explore the hypothesis that the environment offered by a tourist-aimed elephant back safari park may be one which provides the elephant’s needs. To
  • 7. 7 test this hypothesis both physiological i.e. glucocorticoid and observational i.e. behavioural measures of stress were used. Material and Methods The study design is based on the two questions proposed by Dawkins (2008): Q1: “Are the animals healthy?” Q2: “Do the animals have what they want, as defined by what they find positively reinforcing?” Validated outcome measures were used, that is on measures of behaviour and physiology of the elephants, to test these questions (Broom & Johnston 1993; Appleby & Hughes 1997; Wechler 2007).
  • 8. 8 1. Materials: the elephants Six tamed and trained African elephants aged 9 – 26 years were the subject of the study. Data collection entailed observing each elephant’s behaviour and the collection of faecal samples. Details of each African elephant are presented in Table 1. Table 1: Six elephants from the elephant safari company. Elepha nt S e x A g e Captur ed N u m be r of tr an sl oc ati on s M on th s at EF AF M oo ke tsi Arrive d at Eleph ant Whis pers Boma size (m²) Level of tourist human contact Thembo M 27 03/11/27 3 30 08/04/29 42m² High level of contact Ziziphus M 15 06/04/17 3 17 08/04/29 84 m² Moderate level of contact Medwa M 15 06/04/17 2 20 07/12/05 42 m² High level of contact Shimwari M 15 05/07/13 2 29 07/12/05 42 m² Moderate level of contact Lindiwe F 10 06/04/17 2 20 07/12/05 42 m² High level of contact Andile F 14 07/03/08 2 23 09/04/16 42 m² Moderate level of contact
  • 9. 9 Table 2: Elephant-tourist interactions. Excursion Duration Times Description Elephant interaction 1 hr 09:00 12:00 16:00 • Brief history of each elephant. • Demonstrating how elephants are trained • Medwa interaction: interpretation on elephants, clients allowed to offer treats and take pictures, touch Medwa while he’s laying down • Thembo interaction: interpretation on elephants, clients stand between his legs for a picture. • Lindiwe interaction: interpretation on elephants, clients are asked to give Lindiwe commands and to reward her with a treat when she responds correctly. Interaction and ride 1 hr 30 min 09:00 12:00 16:00 • Interaction as described above • Ride: 2 people on each elephant, 20 min long Ultimate Interaction and ride 2 hr 30 min 12:00 • Interaction and ride as described above • Elephants bath in water hole; clients enjoy lunch on deck watching. Early morning wake up, and elephant back ride. 2hr 06:30 • Clients are taken to the Stables • Grooms open stables of elephants • Clients are allowed to brush elephants down • Interaction and ride as described above Sunset interaction, elephant back ride 2hr 16:00 • Interaction and ride as described above • Clients are taken to the Stables * Treats and barna grass are offered to the elephants during interactions. All the elephants received an examination by a veterinary surgeon to confirm that they were in good physical health. 2. Methods: The aim of this study was to assess a correlation between human handling and the occurrence of stereotypical behaviours and potential changes in adrenocortical activity in six trained
  • 10. 10 African elephants used by an elephant safari company in South Africa. Two studies were done over a period of one year. Both Physiological and behavioural outcomes were measured, since periodicity of cortisol release and other hormones which interact and affect the adrenocortical system may influence findings (Dawkins. 1980). 2.1 Glucocorticoid sampling and measuring: The enzyme immunoassay (EIA) technique was used to measure the faecal glucocorticoid metabolites in the elephants according to the procedure described by Viljoen et al (2008) and Ganswindt et al (2005 b). Faecal samples were collected as soon as possible after defecation from the individual elephants. One sample from the six elephants was collected during any of the interaction excursions at 09h00, 12h00 or 14h00. Rubber gloves was used to collect roughly 100 grams of homogenous faecal material from the middle of the bolus to avoid cross-contamination with urine or other faecal samples and then placed in a labelled glass container with an air tide lid. All faecal samples were frozen within 2 hrs of collection and stored at -8 °C until analysis at the Endocrine Research Laboratory of the University of Pretoria. Each sample was marked with the date of collection, time of collection, and the name of the elephant. Faecal samples was collected once a week over demanding and subtle tourism phases, which allowed us to determine, through concentrations of immunoreactive glucocorticoid metabolites, whether the interaction activities with tourist have any possible disruptive influence on an elephant’s normal physiological stability. Samples were collected from December 2009 until September 2010. At the end of each month an outline of the tourist- elephant interaction excursions were documented. Faecal samples were lyophilized, pulverized, and sieved through a mesh to remove undigested faecal matter as described by Fieß et al (1999). An approximate 0.05 g of the faecal powder was then extracted by vortexing for 15 min with 80% methanol in water (3 mL). Following centrifugation for 10 min at 3,300g, supernatants was transferred to a glass tube and then ready for hormone analysis. Faecal extracts were measured for immunoreactive glucocorticoid metabolites using an enzyme immunoassay for 3α, 11oxo-cortisol metabolites (3α,11oxo-CM) (Möstl et al. 2002), which has previously been shown to provide reliable information on adrenocortical function in the African elephant (Ganswindt et al 2003, 2005).
  • 11. 11 2.2 Behavioural study: The observer performed observations during interaction excursions once a week for each elephant (see Table 1) which were recorded on a prepared check sheet (Appendix 1) based on the ethogram drafted by Gruber et al (2000). The instantaneous scan sampling technique (Altmann, 1974 & Martin and Bateson, 1993) was used at 5 minute intervals. All behaviour identified was allocated to one of the seven activity states. These are aggression, comfort, ingestion, locomotion, resting, social and stereotypies (Gruber et al. 2000). To identify behaviour that was thought to be normal behavioural studies were conducted while the elephants were foraging as well as while they were in the stables. The same types of behaviour were recorded as with the interactions. 3. Results: 3.1. Glucocorticoid analysis: A number of variables were considered and models were fitted to determine the relationships between variables and faecal cortisol levels. A number of elephant related variables were considered being Animal, Age, Sex, Dominance ranking, and length of training. When models were run using these variables many were auto correlated and the animal name was retained in the model. Variables considered determining whether interactions are affecting GCM values were no of people taking part in the interaction this was classed to be small groups which consisted of groups less than 30 people and large groups > 30 people. Nr of Interactions and nr of Rides in the 25 hours period before the GCM sample was taken were also recoded as well as the number of interactions that had less than 2 hours in between interactions as the assumption here was that if the foraging time between Elephants was reduced that they could be more stressed. Environmental variables considered were Rainfall and Month of year. A 164 (mean 27 samples per individual) faecal samples were collected between December 2009 and September 2010 and FGM concentrations were successfully obtained.
  • 12. 12 Linear regression models were used to predict the relationships between faecal cortisol levels and the variables mentioned above. When fitting these models the constant error variance assumption was violated a small p value was obtained and there was an indication of clumping in the centre as well as funnelling at larger values. To correct for this Generalise Least Square (GLS) approaches were used. GLS assumes a different relationship between the residual variance and the fitted values. Figure 1: Median GCM levels for the 6 different Elephants There was no correlation between age and FGM concentrations, as discovered by Munshi- South et al (2008) where adults have significantly higher FGM concentrations than juveniles. Dominance ranking were not correlated with FGM levels as previously revealed by Ganswindt et al (2005), where FGM concentrations during periods of aggressiveness were significantly lower than those of animals in a nonaggressive condition. The concentrations of FGM in the six African elephants were not influenced by seasonal changes. There was no elevation of concentrations of FGM during the dry season as Andile Lindiwe Medwa Shimwari Thembo Zizi
  • 13. 13 previously discovered by authors (Foley et al 2001; Ganswindt et al. 2005; Rasmussen et al. 2008, Viljoen et al. 2008b, Ganswindt et al. 2010). This could be due to the high quantity and nutritional value of food provided to the elephants. Codron et al (2006) stated that the percentage of nitrogen in elephant faeces from the southern KNP showed a significant increase from the dry to the wet season. An elevation of nitrogen in faeces is known as a useful indicator of nutristional status. There was no significant correlation between FGM levels and the sex of the elephant; but Andile’s FGM concentration profile tend to have a inclination towards a cycling female elephants progestogen profile (Brown, 2000). Foley et al (2001) established that cortisol metabolite and progesterone concentration are significantly correlated. However, this is not conclusive and progesterone and FGM values needs to be assessed simultaneously, through weekly collection of faecal samples The number of rides became significant at the 10% level. When one looks at interaction plots below the first one showing the Elephant name, GCM value and the Nr of Rides, one can clearly see that there is a significant variation in the cortisol values between the elephants. Andile has the highest GCM value all the time and the effects that one may expect to see could, with the different number of rides, be reduced because of the inter elephant variation. One needs then to compare each elephant to itself and unfortunately the amount of data will not allow us to do this. For example Lindiwe, who has the lowest cortisol value, has the biggest effect when a second ride is added.
  • 14. 14
  • 15. 15 A similar effect was apparent when the number of interactions was analysed. Andile, once again has the highest levels. Lindiwe the lowest and there is quite a marked increase in Lindiwe compared to the others. It therefore appears that the individual elephant itself has the greatest effect on the cortisol levels and if one would like to start looking at different interaction group and ride sizes one may want to only look at the highest and lowest elephant and get a large samples size for these. How each elephant respond to the interactions and rides can be reflected in their mean FGM concentrations, each elephant are different from another elephant. The rise in FGM concentration and the number of interactions: Elephant Mean FGM concentration from 1 to 2 interactions Mean FGM concentration from 2 to 3 interactions Lindiwe Increases 1,26 fold Increases 1,03 fold Shimwari Decreases 0,99 fold Decreases 0,9 fold Medwa Increases 1,17 fold Decreases 0,83 fold Thembo Increases 1,29 fold Decreases 0,84 fold
  • 16. 16 Andile Increases 1 fold Decreases 0,89 fold Ziziphus Increases 1,03 fold Increases 1,01 fold The rise of FGM concentrations correlates with the number of rides Elephant FGM concentration when more than 1 ride Lindiwe Increases 1,24 fold Shimwari Decreases 0,98 fold Medwa Increases 1,03 fold Thembo Increases 1,06 fold Lindiwe Increases 1,06 fold Ziziphus Increases 1,05 fold Taken as a whole, FGM concentrations increased 1, 12 fold when a second interaction occurred. When a third interaction occurred FGM concentrations in Lindiwe and Zizi increased 1, 02 fold more, but decreased 0, 87 fold in the other 4 elephants. Lindiwe’s shows a more significant respond to interactions, but she has the lowest mean FGM concentrations.. FGM levels increased 1, 09 fold when more than one ride occurred, but FGM levels in Shimwari decreased 1, 09 fold. Again Lindiwe is showing higher response, but still has the lowest mean FGM concentrations. The number of interactions and rides seems not to have a significant correlation with mean FGM concentrations in elephant. Each elephant has a unique FGM. Behavioural analysis: The observational data was lumped across all the Elephants since the number of observations taken from the three different activities were not equal. Proportions were calculated for each type of behaviour and these were then totalled over the different categories above to get one
  • 17. 17 proportion per category. A student t test was then used to calculate whether there were significant differences between the observations observed in the different activities. Between-observer reliability was measured to determine the accuracy of behaviour definitions used within each category. An interaction excursion was randomly selected and the two observers independently measured each elephant’s behaviour at 5-minute intervals for the entire excursion using the Gruber’s et al ethogram (Table 1). An index of concordance, comparing the total number of agreements (A) and disagreements (D), were performed using the formula I = A/ (A+D) (Martin and Bateson, 1993). Within-observer reliability was measured to determine whether there is any “observer drift” during the duration of the study. An interaction excursion was selected at random, and on two separate occasions the same observer measured each elephant’s behaviour at 5-minute intervals using the Gruber’s et al ethogram (Table 3). An index of concordance was then be performed using the formula I = A/ (A + D) (Martin and Bateson, 1993). The results from both studies were compared. evaluated with baseline concentration of faecal glucocorticoid metabolites in captive and free-ranging African elephants (e.g Ganswindt et al 2003; 2005a; b; 2009; Viljoen et al., 2008 a; b) and against known behavioural indicators of stereotypies in captive elephants identified by Garaĭ (1997) and Gruber et al (2000). Physical variables: geographic range and body size. The six trained African elephants are kept in a 4000 hectare conservancy located in the Lowveld’s savanna, which is analogous to geography of the Kruger National Park. Husbandry of the six elephants is currently under the supervision of the Department of Environmental Affairs and Tourism (DEAT). The boma layout consists of seven 42m² stables and one 84m² stable for Thembo (3m in shoulder height) and is assembled with 4m gum poles 200mm diameter thick under a corrugated roof. The design is open, well ventilated and allows the elephants to release excess heat into the atmosphere they store above 23 C as Langman advices (1990). The elephants also have complete visual and tactile contact amongst each other, as articulated by Clubb & Mason (2002).
  • 18. 18 The floor of each stable is rounded to allow adequate runoff into a furrow and is often treated with an organic insecticide. The top layer of the floor is regularly removed and replaced with new soil. The elephants enter the stables at 17:30 and are provided with bedding and fresh cut branches from indigenous trees at 18:00 and 24:00 and let out at 07:00. Fresh drinking water is kept in a reservoir outside the stables. The elephants are able to drink and splash themselves with water before they go into the stables in the evening and in the morning before starting their day. Water was kept in their stables, but the elephants played more with it than drinking it which created mud pools in their stables. Cleaning of stables starts soon after the elephants have left their stables, the dung is moved to a compost heap and the left over branches are first deposited into a chipper and then thrown onto the compost heap, to decrease exposure to potentially dangerous compounds from faeces and urine (Veasey, 2006). After their morning training and exercise session, the elephants are allowed to roam free in the 4000 hectare conservancy, while watched over by four grooms. The elephants are brought together at the interaction site when there is a tourist interaction. The six elephants are able to shed excess body heat between interactions in the rivers and waterholes, and during interactions, if they require it, can be drenched with hose water. The exhibit and conservancy provide elephants with environmental options that allow them to regulate their body temperature effectively as recommended by Langman’s (1990, 1996, 2003) and Rees’s (2002) research. The stables are in proximity to a public road, and there are sometimes large trucks driving past. Occupational variables: activity cycle and habitat use.
  • 19. 19 There is a specific activity routine set out for the elephant’s everyday. The day start 07:00, the elephants are let out of the stables and move towards the reservoir for a drink and a splash of water. Before free ranging, a 20 minute exercise activity is conducted. Depending on the bookings, tourist interactions are at 09:00, 12:00 and 16:00, which last approximately 2 hours each (sometimes only one or two interaction is done per day). Elephants free range between interactions. Elephant are taken back to stables at 18:00, and allowed to drink and splash water, and immediately provided with fresh cut browse, which is in small piles outside the stables, they are again fed at 21:00 and 24:00. The activity sketch of these elephants is polycyclic. The elephants occupy more or less 18 hours of their day browsing or grazing. They are in motion almost continuously while feeding. The rest of their day is mostly given over to socializing, water or dust bathing, or wallowing in mud. They rest for about 4 hours a day, either in a recumbent or in standing position only in their stables. This occupational pattern is analogous to their cohorts in the wild (Moss, 1988; Eisenberg 1981). There are many options accessible to the six captive elephants permitting them to maintain a natural activity pattern. The habitat of the conservancy can be described as dense bush on the uplands, open tree savanna in the bottomlands with waterholes and mud pools, and dense riverine woodland on the river. It is 4000 hectares, greater than suggested by Hutchins (2006) necessary for elephants in captivity. Options to the elephants include space to roam on a variety of substrates, with a variation in topography, and access to suitable plant material or substantial and free provision of cut fresh browse (branches) for species specific foraging. They have daily access to water and mud of adequate volume to allow totally submerged bathing and all-body wallowing. A total of 135 observations were performed with an average length of 30 minutes between January and September 2010. Two students t tests were conducted the first one to determine whether there was a significant difference in the behaviour recorded during the interactions and while the Elephants Foraged and the second one was between the Interactions and when they were in the stables. Both of these tests showed that there are no significant differences in behaviour. The graph shows the different proportions that were recorded in each different behaviour category
  • 20. 20 0 10 20 30 40 50 60 Aggression comfort ingestion locomotion resting social stereotypies forage interactions stables Fig. 4. The effect of forage, interactions and stables on behaviour. The percentage of observation performing each activity was determined for each elephant during interaction. 0 10 20 30 40 50 60 aggression comfort ingestion locomotion resting social stereotypies medwa lindiwe shimwari andile thembo Zizi Discussion This study has demonstrated, we believe for the first time, that FGM concentrations in captive elephants exposed to daily tourist activities fall within the ‘normal’ range previously Behavior % % Behavior
  • 21. 21 recorded for African elephants living in the wild. Around the Samburu and Buffalo Springs National Reserves, Kenya, 64 individual bulls showed FGM concentrations from 0.2 GCM (µg/gDW) to 2 GCM (µg/gDW) (Fig. 2 in Ganswindt et al., 2005). In the present study it appears that the number of interactions or rides do not demonstrate a significant physiological challenge to the elephants. Elephants can acclimate to disturbed/ unnatural environments, as found by Munshi-South et al (2008), where they found the African elephants in Loango National Park exhibited significantly higher FGM concentrations than elephants in a industrial corridor dominated by oil fields. As previously observed by other authors, usually only severe stressors are found to have significant effects on cortisol concentrations similar to those measured after ACTH administrations (4 -5 fold increase; Ganswindt et al., 2003). Mean FGM concentrations associated with translocation increased 6-7 fold (Viljoen et al. 2008a, Millpaugh et al. 2007) and with episodic loud noices increased 3 – 4 fold. FGM concentrations in 2 physically injured free-ranging African elephants increased 3 fold (Fig. 2 in Ganswindt et al., 2010). Seasonal variance in FGM concentrations of African elephants increased more than 2 fold between regular seasons (Foley et al. 2001, Viljoen et al. 2008b). Glucocorticoids (GC’s) are a classic endocrine response to stress. Despite that, it remains litigious as to what purpose GC’s serve at such times. The tendency to think that the stress axis is only a response of the body to short-term stressors is wrong, since it also plays a key role to carry out the daily functions of living (McEwen 2001). It is associated with the diurnal cycle of waking such as increased locomotion, increased appetite, exploratory behaviour and food-seeking behaviour (reviewed by McEwen et al, [1998], Reeder & Kramer [2005], and Wingfield & Romero [2001]. Dallman and colleagues found that glucocorticoid concentration has a pronounced circadian rhythm, being highest at the onset of daily activity and lowest at the end of it. Behaviourally the elephants spent more time in comfort, ingestion and locomotion activities than in social and resting activities. Stereotypies barely occurred and there were no occurrences of aggression. Stereotypic behaviours are generally considered as indicators of poor welfare (Kiley – Worthington 1990; Gruber et al 2000). Gruber et al (2000) studied the effect of penning and chaining on circus elephants and found stereotypies accounted for 20 - 45 % of the behaviours. Similar behaviour was found in other studies. In Sri Lanka, weaving in circus elephants, were whenever they had to wait for something or where expecting
  • 22. 22 something. They increased the frequencies of weaving before they were fed or when they were expecting water. Elephants observed during the Kandy Perahera weaved before they were fed (Kurt & Garai, 2001). Stereotypic behaviours help the animal cope with unpleasant stimulation or boredom and animals performing these behaviours therefore have lower heart rates and reduced cortisol levels than not-stereotypic animals under the same conditions (Clubb & Mason, 2002; Veasey, 2006). They engaged in a full range of natural behaviours also seen in wild elephants (Clubb and Mason 2002). Their mean faecal glucocorticoid metabolite concentrations were similar to wild elephants, except that their mean FGM levels do not elevated during the dry season as found in wild elephants (Foley et al. 2001; Rasmussen et al 2008; Viljoen et al. 2008b; Ganswindt et al 2010). The elephants did not exhibit behaviours of aggressive or stereotypies as seen in elephants under stress (Garai, 1997; Hutchins, 2006, Clubb & Mason, 2002). It also appears that the elephants experience human handling positively, since they continue to do the activities willingly. Olson substantiates: “behaviour does not occur as isolated and unrelated events; the consequences that follow the actions of an elephant, whether good, bad, or indifferent, will have an effect upon the frequency which those actions are repeated in the future.” “All reinforcement increases the likelihood of a behaviour being repeated.” The positive reinforcers seem to be the combination of getting attention, being praised and getting a reward. The elephants seem to have control over their own behaviour. This is exceptionally important since research on stress specifies that the ability to exercise control over an environment, even if the stress stimulus cannot be removed, exceedingly lowers the degree of stress experienced by the animal (Seligman et al. 1977; Foster-Turley et al 1982; Markowitz et al 1989; and Laule and Desmond 1998). 1. Conclusion This paper, for the first time, suggests that the hypothesis that wild elephants trained and kept in back-safari tourist parks do not experience undue stress from the experience. It is important however to highlight the large size of the park and the focus on the welfare of the elephants demonstrated by the park staff.
  • 23. 23 The study results support the following recommendations to establishments managing trained elephants in close contact with tourist: 1) the elephants must occupy a large enough habitat providing conditions promoting species- appropriate behaviour as revealed by this species’ natural history (Mench and Kreger 1996, Hancocks 1996; Coe 2003). 2) Herd mates must be compatible, which is a highly effective form of enrichment and therefore important (Hutchins, 2006; Veasey, 2006). 3) The elephants must not experience any unnecessary pain or distress. 4) A training regime predicted on positive reinforcement and respect for the animal’s autonomy is best suited to enhance the lives of the elephants and providing for their psychological well-being. 5) A routine activity pattern so that the elephants can learn what to expect next. Elephants will have a sense of control over their environment and are required to make less abnormal or extreme adjustments in their physiology or behaviour. (Friend, 1980; Carlstead, 1996; Mason, 1991). 6) Elephants must be able to partake in species-typical behaviours, even when they are interacting with tourist or when they are in stables. 7) Monitoring the faecal glucocorticoid metabolite in conjunction with behavioural observation is a useful diagnostic tool to understand how elephants respond to training and interacting in close contact with humans. Acknowledgements Special thanks to Andre Kotze, who supervises the care and guidance of these elephants, and the elephant handlers at Elephant Whispers, for their support and assistance. The author thanks Rory and Lindi Hensman from Elephants for Africa forever, for their background information on these elephants. The author is grateful to Dr Andre Ganswindt for providing access to the reagents of FGM enzyme immunoassays and Stephany Münscher for expert help in laboratory techniques. The author is also grateful to Judith Botha, Dr. Andre Ganswindt and Dr. Anje J Higgo for reviewing the manuscript, with special thanks to Judith
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