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The Elephant who Finally Crossed the Road – Significant Life Events Reflected in Faecal Hormone Metabolites of a Wild Asian Elephant

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We used GPS-telemetry and faecal glucocorticoid metabolites (fGCM) to monitor a wild translocated female elephant in rainforests of Peninsular Malaysia. The elephant was GPS-tagged at translocation and her fGCM monitored within 11–22 months after translocation. The lowest fGCM concentrations were observed at the beginning of hormone monitoring, when she exhibited unusual movement patterns, moving repetitively alongside a major road without crossing it. Around the 16th month after translocation, the elephant delivered a calf and in the 18th month she crossed the road. In this period, she exhibited increased fGCM concentrations, presumably indicating response to challenging life events
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The Elephant who Finally Crossed the Road – Significant Life Events Reflected
in Faecal Hormone Metabolites of a Wild Asian Elephant
Article · September 2018
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Salman Saaban
Department of Wildlife & Nat. Parks Peninsular Malaysia
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Jamie Wadey
University of Nottingham, Malaysia Campus
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Introduction
It is challenging to study elusive Asian
elephants (Elephas maximus) in the rainforest
due to the dense foliage and limited sightings
(Blake & Hedges 2004). Recent technological
developments, such as GPS-telemetry and non-
invasive molecular techniques, have considerably
improved the wildlife ecologist toolbox and our
capacity to study forest elephants. Similarly,
ability to measure hormone metabolites from
faeces, allows the physiological monitoring of
free-ranging wildlife without the need to capture
the animal.
Glucocorticoid hormones play a role in
modulating daily energy needs and in helping
to prepare the body to cope with challenges,
managing the period of stress and in recovering
after the challenge has passed (Sapolsky et al.
2000). Wildlife biologists can now use faecal
glucocorticoid metabolites to gauge wildlife
Peer-Reviewed Research Article Gajah 48 (2018) 4-11
The Elephant who Finally Crossed the Road – Signicant Life Events Reected in
Faecal Hormone Metabolites of a Wild Asian Elephant
Ee Phin Wong1,2,*, Lisa Yon2, Susan L. Walker3, Alicia Solana Mena1, Jamie Wadey1,
Nasharuddin Othman4, Salman Saaban4 and Ahimsa Campos-Arceiz1,5
1School of Environmental and Geographical Sciences, Faculty of Science,
The University of Nottingham Malaysia, Jalan Broga, Semenyih, Selangor, Malaysia
2School of Veterinary Medicine and Science, Faculty of Medical & Health Sciences,
The University of Nottingham, Sutton Bonington, Leicestershire, UK
3Chester Zoo, Upton-by Chester, Chester, UK
4Department of Wildlife and National Parks Peninsular Malaysia, Kuala Lumpur, Malaysia
5Mindset Interdisciplinary Centre for Environmental Studies,
The University of Nottingham Malaysia, Jalan Broga, Semenyih, Selangor, Malaysia
*Corresponding author’s e-mail: eephin@gmail.com
Abstract. We used GPS-telemetry and faecal glucocorticoid metabolites (fGCM) to
monitor a wild translocated female elephant in rainforests of Peninsular Malaysia. The
elephant was GPS-tagged at translocation and her fGCM monitored within 11–22 months
after translocation. The lowest fGCM concentrations were observed at the beginning of
hormone monitoring, when she exhibited unusual movement patterns, moving repetitively
alongside a major road without crossing it. Around the 16th month after translocation, the
elephant delivered a calf and in the 18th month she crossed the road. In this period, she
exhibited increased fGCM concentrations, presumably indicating response to challenging
life events.
responses towards anthropogenic impacts such
as tourism, logging, and translocation (Wasser et
al. 1997; Thiel et al. 2008; Dickens et al. 2010;
Wong 2017). In addition, it is considerably easier
to obtain faecal samples in the eld than saliva,
urine, or blood (Palme et al. 2005), as wild Asian
elephants are known to defecate up to 18 times
per day (Hedges et al. 2005).
Furthermore, faecal glucocorticoid metabolites
(fGCM) patterns are reective of free gluco-
corticoid concentrations in the blood, after taking
into account the gastrointestinal transit time
(Touma & Palme 2005; Sheriff et al. 2010a), and
are therefore a reasonable method to evaluate
adrenal activity. However, the use of fGCM,
requires various validation tests to ensure we are
measuring actual adrenal responses instead of
environmental or sampling artefacts (see reviews
by Millspaugh & Washburn 2004; Goymann
2012). In previous studies, we have validated
the use of fGCM in Asian elephants (Watson et
© 2018 The Authors - Open Access
5
al. 2013) and that fGCM samples are stable up
to eight hours after defecation in a tropical rain
forest environment (Wong et al. 2016).
In 1950, Selye introduced his theory of “General
Adaptation Syndrome” outlining the adrenal
glands’ role in secreting glucocorticoids as
response to stimulants (stressors). Since then,
more researchers have identied links between
glucocorticoid concentrations and health. In
a “ght or ight” scenario when faced with a
dangerous situation (e.g., zebra chased by a
lion; Sapolsky 2004), within seconds to minutes,
the body will release a cascade of hormones,
including catecholamines and corticotropin-
releasing hormone (CRH), into the blood stream;
these effect a number of physiological changes
in the body (Sapolsky et al. 2000; Sheriff et al.
2011). The CRH, secreted by the hypothalamus,
stimulates the pituitary’s secretion of
adrenocorticotropic hormone (ACTH), which in
turn, will stimulate the adrenal glands to release
glucocorticoids minutes after the stressful
encounter (Chrousos 1998; Sapolsky et al. 2000;
Sheriff et al. 2011).
Glucocorticoids are steroid hormones that will
exert a physiological effect on the body over
a few hours, and will act through a negative
feedback loop to receptors in the brain, to reduce
the production of CRH and ACTH after the
stressor ends (Sapolsky et al. 2000). In an acute
stress scenario, glucocorticoids play a vital role
in managing stress and assisting in recovery
from stressors (Sapolsky et al. 2000), which
includes mediating immune responses to prevent
overshooting or autoimmunity, enhancing
cardiovascular activation during stress, and
maintaining the sensitivity of β-adrenergic
receptors to catecholamines at vital locations in
the body, including the heart (McEwen 1998;
Sapolsky et al. 2000; Silverman et al. 2005).
Although glucocorticoids are often termed as
“stress hormones”, they have important functions
outside the “ght and ight” stress response. Basal
glucocorticoids have a circadian cycle in our body
and play an important role in energy regulation. At
low to moderate levels, glucocorticoids stimulate
appetite; and appetite normally peaks when basal
glucocorticoid concentrations are at their highest
early in the morning (Sapolsky et al. 2000).
When acute stress occurs, appetite is suppressed
temporarily (less than an hour) and afterwards
glucocorticoids may help build appetite to
encourage metabolic intake and prepare the
body for subsequent stressors (Sapolsky et al.
2000). If the timing and secretion pattern for
glucocorticoids are disrupted (McEwen et al.
2015), the adrenal response is impaired (Dickens
et al. 2009), or the body reaches exhaustion due
to chronic stress (Selye 1950; Sapolsky 1999),
then there could be negative impacts on health.
Elevated glucocorticoids can have adverse
effects on memory, learning, and cognitive
function (Sapolsky 1999; McEwen et al. 2015).
Although not so well known, low concentration
of glucocorticoids is linked to acute adrenal crisis
(a potentially life-threatening condition; Lee &
Ho 2013), chronic fatigue syndrome (Edwards
et al. 2011), and post-traumatic stress disorder
(Raison & Miller 2003; Yehuda & Seckl 2011),
amongst other health problems (Heim et al. 2000;
Cicchetti & Walker 2001). Therefore, the ability
to maintain an adequate concentration of basal
glucocorticoids is vital for the body in managing
daily activities (Sapolsky et al. 2000; Busch &
Hayward 2009; Madliger & Love 2014), as well
as in facing stressors or energy-intensive life-
history stages such as migration (Sapolsky et al.
2000; Wingweld & Kitaysky 2002; McEwen &
Wingweld 2003).
Peninsular Malaysia is home to an estimated
population of 1223–1677 wild Asian elephants
(Saaban et al. 2011) that, like elsewhere in the
species range (Fernando & Pastorini 2011),
are endangered due to the combined effect of
habitat loss and human-elephant conict (HEC).
Translocation, moving elephants from conict
zones to protected areas, has been one of the
main strategies to mitigate HEC in Peninsular
Malaysia in recent decades, with approximately
10 to 25 wild elephants translocated every year
since 1974 (Saaban et al. 2011; pers. comm.
Nasharuddin Othman). Not much is known about
the impact of translocation on elephants, nor how
they fare after their release. The work presented
here is part of the activity of the Management
and Ecology of Malaysian Elephants (MEME)
6
project, a collaboration between university
researchers and local wildlife authorities that
aims to move towards an evidence-based
conservation of elephants in Peninsular Malaysia
(http://www.meme-elephants.org). Among other
activities, MEME is using GPS-telemetry and
fGCM monitoring to study elephant response to
translocation, comparing the movement patterns
(e.g. Wadey et al. 2018) and hormone proles
(Wong 2017) of translocated and local resident
elephants at release sites. Here we present a case
study that uses movement tracking and hormone
proles to gain insights into the physiological
condition of a wild elephant.
Methods
Study site
The Belum-Temengor Landscape (BTL) is
located in the northwest of Peninsular Malaysia
(Fig. 1), and is mainly comprised of hill
dipterocarp and upper dipterocarp forest. It
covers the Royal Belum State Park (1175 km²),
Temengor Forest Reserve (1489 km²), state land
(131 km²), indigenous villages, plantations,
rivers and a large dam (Rayan & Linkie 2015).
This landscape is bisected by the Gerik-Jeli East-
West highway, of about 121 km in length (Wadey
et al. 2018).
Study subject
The elephant in this case study is a female (named
Mek Jalong) from the south of Perak that was
translocated 94 km to BTL on the 20th May 2012
(day 0). Jalong was tted with a GPS-satellite
collar (~17 kg, Africa Wildlife Tracking, South
Africa), which tracked her movements every
two hours from day 0 to day 669. We started
monitoring Jalong’s fGCM in the 11th month
(day 341) after her translocation and stopped in
the 22nd month (day 669), when her GPS-collar
failed. During this latter period (days 341–669),
Jalong underwent two presumably challenging
(in terms of stimulation of the HPA axis) events.
The rst event was the birth of her calf (Fig. 2),
which took place around the 16th month after
translocation. This indicates that Jalong was four
to six months pregnant when she was translocated.
The second event was when she crossed the East-
West highway for the rst time during the study
period, 18 months (day 537) after translocation.
Field sample collection
We tracked Jalong on the ground by rst using
the GPS collar’s location coordinates to know
where she had been in the previous few hours
and, then, using the strength of the collars VHF
signal and forest signs (e.g. footprints, disturbed
Figure 1. Combined tracklog (days 0–660) of Mek Jalong’s movement before (blue dots) and after
(yellow dots) crossing a major highway (black line) in the Belum-Temengor landscape for the rst
time on day 537 after translocation.
7
vegetation, and the sound of apping ears and
feeding) to narrow down Jalong’s position. Once
the tracking team was at close distance from
the elephant (within visual or auditory range),
we closely tracked her movements to look for
fresh dung assumed to have been produced by
her. Since the elephant never joined any other
elephant (except her calf) and we were tracking
her at very close range, it is highly unlikely that
the dung samples we collected could have been
produced by any other elephant. Once we found
a dung pile, we recorded the GPS location and
environmental variables associated.
The faecal samples were collected using clean
surgical gloves and stored in a zip-lock bag;
approximately 100 g of faecal material was
removed from the middle of the bolus from an
average of three intact boli. The fGCM samples
were mixed thoroughly in the zip-lock bag and
placed immediately in a cooler bag with ice
packs, before transferring it to a portable car
compressor freezer (–15°C to –18°C; Mobicool
CF18C and CDF-11, Germany, powered by
car AC socket) or chest freezer (–20°C) at our
eld station. Following Wong et al. (2016), only
samples stored in the freezer within eight hours
after defecation were used in the analysis.
In the 11 months in which we monitored Jalong’s
fGCM, we obtained a total 13 dung samples from
nine different sampling occasions.
Laboratory analysis
We used a wet-weight extraction technique
(Watson et al. 2013), whereby 5 ml of 90%
methanol were used to extract fGCM overnight
from 0.5 g (± 0.003) of a well-mixed dung
sample. Extracts were dried and reconstituted
in 1 ml of 100% methanol, and stored at –20°C
until being analysed with a corticosterone
enzyme immunoassay (CJM006, Coralie Munro,
UC Davis). The biological and biochemical
validation for the assay was previously carried
out by Watson et al. (2013). Only data with an
intra-assay coefcient of variation (CoV) of less
than 10% and inter-assay CoV less than 15%
were used for subsequent analyses.
Results
In the approximately 16 months after her
translocation, Jalong remained solitary although
there were other elephant groups in the area.
She moved up and down repetitively along the
northern side of the East-West highway, always
close to the road but never crossing it (Fig. 1).
When Jalong’s fGCM monitoring started on day
341 post-translocation, for 4.5 months, Jalong’s
mean fGCM was 7.3 ± 1.2 ng/g (SD; Fig. 3).
Jalong was rst noticed to be with her calf on day
481 post-translocation during a eld track. Soon
after that (day 536), Jalong crossed the East-
West highway for the rst time (Fig. 1). In the
period between these two events, Jalong’s fGCM
uctuated (mean±SD fGCM = 10.9 ± 3.9 ng/g;
Fig. 3). We recorded Jalong’s highest fGCM
value shortly before she crossed the highway
(15.9 ng/g, highest concentration throughout the
monitoring period of 11 months). After crossing
the highway, Jalong’s movement changed and
she began exploring new areas away from the
road (see Fig. 1), while her fGCM concentration
persisted around 11.2 ± 1.4 ng/g for the remaining
four months (Fig. 3) until monitoring terminated
at day 669 post-release, when the GPS satellite
housing detached from the collar.
Discussion
At the beginning of the study, Jalong roamed alone
and showed repetitive movements alongside the
highway (i.e. she seemed attracted to the highway
Figure 2. Mek Jalong and her newborn calf.
8
but avoided crossing it). This is a very unusual
movement pattern compared to other elephants
monitored in this landscape (Wadey et al.
2018). Jalong’s initial fGCM concentration was
similar to fGCM concentrations found in other
translocated elephants in the year immediately
after translocation (8.5 ± 1.9 ng/g, N = 5; all
males; Wong 2017) but lower in comparison to
local resident elephants in the same landscape
(11.4 ± 2.8 ng/g, N = 4, 3 males and 1 female;
Wong 2017). Although the East-West highway
has a negative impact on elephant movements in
the area, the elephants in the landscape are still
able to cross it. Wadey et al. (2018) found that
translocated elephants in this landscape were
14 times less likely to cross the road than local
ones, suggesting that road crossing is particularly
challenging to elephants not familiar with the
road. In separate studies, we have found that wild
elephants are attracted to this highway due to the
availability of grasses and other early succession
plants, mainly monocots, in the area (Yamamoto-
Ebina et al. 2016; Terborgh et al. 2017).
Before Jalong crossed the highway for the
rst time, we detected an increase in fGCM
concentrations. The time of the road crossing
event, however, also coincided with Jalong’s
delivery of her calf, which also may result in an
increase in fGCM concentrations (Brown 2000).
Jalong’s fGCM concentration remained elevated
after crossing the road; this could be related to
the challenges of exploring a new environment
(there was a change in movement patterns and
Jalong was exploring areas further away from
the road) and the need to be vigilant when caring
for offspring (Rees et al. 2004). Jalong’s fGCM
concentration values, which persisted after
crossing the highway, however, were within the
usual fGCM range for local elephants in the area
who crossed the highway regularly (Wong 2017).
In retrospect, the increase in fGCM in Jalong’s
case could be due to many other reasons, but
we speculate it is a positive indication that she
was actively coping with challenges in her
surroundings and in caring for her young calf.
Although there could be innate fGCM differences
between male and female elephants, both will
respond to challenging situations in the eld and
show an increase in fGCM (Vijayakrishnan et al.
2018).
The unusual nature of Jalong’s movements
before crossing the road and her relatively
low fGCM concentration compared with local
elephants in the landscape (Wong 2017) could
be of concern, since prolonged periods of low
glucocorticoid concentrations can be associated
with health problems (e.g. Dickens et al. 2009;
Linklater et al. 2010; Pawluski et al. 2017). In
future studies, researchers should investigate
the importance of having an adequate amount
of basal glucocorticoids in helping humans
and animals to manage challenges in their
surrounding (Sapolsky et al. 2000; McEwen &
Wingweld 2003).
Alteration of the mother’s glucocorticoid con-
centrations during pregnancy can exert inuence
on her offspring’s (F1) and grandchildren’s (F2)
stress response, physiology, and health (Franklin
et al. 2010; Sheriff et al. 2010b; Matthews &
Phillips 2012; Khan et al. 2016). This also means
that Jalong’s translocation could potentially
affect her calf’s health and behaviour.
This case study demonstrates that (1) GPS-
tracking can be successfully combined with
fGCM to monitor the physiological condition of
wild Asian elephants in tropical rainforest and
(2) signicant life events can be reected in wild
elephants’ fGCM concentrations. Although our
sample size is too small to draw conclusions, our
Figure 3. Faecal glucocorticoid metabolites
prole for Mek Jalong. The red line was drawn
using loess smoothing (span 0.75) and the shaded
grey area represents standard error 95%.
9
results and those in Wong (2017) suggest that
translocation could affect elephants’ health and
behaviour. More research is needed to understand
the relationship between elephant exposure to
prolonged stress and changes in glucocorticoid
concentrations, and when these hormonal
changes can be harmful for the elephants. In this
context, we call for the precautionary principle in
managing wild elephant populations.
Acknowledgements
This study is part of the Management & Ecology
of Malaysian Elephants (MEME), a joint research
project between the Department of Wildlife and
National Parks (DWNP) Peninsular Malaysia
and the University of Nottingham Malaysia.
We are very grateful to DWNP, and especially
to Dato’ Abdul Kadir bin Abu Hashim and
Dato’ Abdul Rasid Samsudin, DWNP’s current
and former Director Generals, for the permits
to conduct this research and for the continuous
support in the eld. Field activities were
generously nanced by grants from Yayasan
Sime Darby (M0005.54.04) and Marinescape
(M0004.54.04). DWNP’s elephant translocation
team and Perak’s elephant unit conducted the
elephant capturing and sedation; Mohammad
Rizal Bin Paimin, Steven Lim, Param bin Pura,
Muhammad Tauhid bin Tunil, Sudin A/L Din,
Rizuan bin Angah, Khairil Othman, Shaharom
and many other individuals provided key
assistance during elephant collaring and tracking
activities. Chester Zoo and their lab technician,
Ms. Rebecca Purcell, have assisted in the setting-
up the faecal endocrinology laboratory at the
University of Nottingham Malaysia Campus that
made the analysis possible. We are grateful to all.
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... Moreover, these appearances are valuable information for nurturing elephant programs that live naturally or domestically (Meytasari et al. 2014). The development of technology nowadays, like GPS (Global Positioning System) and non-invasive molecular technic, helps increase our understanding of observing and studying the wildlife ecology, especially wild elephants (Wong et al. 2018). After that, analyzing the vegetation intensity damage at KPH Kotaagung Utara using the vegetation indexes. ...
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The Indonesian Elephant Conservation Forum stated that the population of Sumatran elephants (Elephas maximus sumatranus) had decreased dramatically up to 70% in the last 20-30 years due to illegal hunting, land conversion, and encroachment, so the availability of elephant food in the wild is gradually inadequate. With the decline of the elephant population in Indonesia, several parties such as the government, NGO, and the public are beginning to monitor the Sumatran elephant. The monitoring is carried out by observing and studying the movements of elephants using a GPS Collar. The research aims to find out the consistency of elephant movement and its relationship to the availability of feed as indicated by the intensity of vegetation in KPH Kotaagung Utara, Lampung Province, Indonesia. This research used GIS technology (Correlation Citra Landsat 8 OLI and BIG Demnas Data), elephant movement data using GPS Collar in 2020, and land use data by BPKH Lampung. The results showed that the monthly movement pattern of elephants in 2020 was consistently monitored. From January-July, elephants are in the North area, while in August-December are in the South. The intensity of elephant movement in the Mixed Shrub Dryland Agriculture area is higher than in the other areas, at 107 points or about 90% of all the areas in KPH Kotaagung Utara. Meanwhile, in the Dryland and Shrub Agriculture areas, there are 6 points each, or about 5% of all the areas. The vegetation classification in KPH Kotaagung Utara is dense with an NDVI value range of 0.63-0.85. Furthermore, the regression results prove that NDVI and the monthly season affect the movement of elephants with a p-value of <0.001.
... Factors including the lack of habitat enrichment activity, essential sources, and other physical factors might cause elephants' avoidance of the bridges. The frequent presence of elephants on the East-West Highway (Wadey et al., 2018;Wong et al., 2018b) and the placement of warning signages for elephants on the road (Timbuong, 2019) show a high tendency for this species to not using the CS. On the other hand, the viaducts were explicitly designed to connect the elephants' main landscapes (Saaban et al., 2011). ...
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The Felda Aring - Tasik Kenyir Road was identified as one of the most threatening roads to wildlife in Malaysia. The present study was conducted to assess the road crossing activities involving the medium- to large-mammal species due to the problem stated. The objectives of this study were to (1) predict the suitability of the road and its surroundings as the roaming areas for the Asian elephant (Elephas maximus, n = 104) and Malayan tapir (Tapirus indicus, n = 66), (2) identify the mammalian species inhabiting the forest beside the road, (3) compare the forest’s common species [photographic capture rate index (PCRI) > 10/ detection probability (P) ≥ 0.05] with the ones utilising the road crossing structures; the viaducts and the bridges, and (4) determine the most impacted species from traffic collisions. The road and its surroundings were classified as moderately suitable to the elephant and tapir (suitability values = 0.4 - 0.8). A total of 16 mammal species were recorded at the forest edges, in which the wild pig (Sus scrofa) (PCRI = 118.96, P = 0.3719 ± 0.027), barking deer (Muntiacus muntjak) (PCRI = 68.89, P = 0.2219 ± 0.0232), sun bear (Helarctos malayanus) (PCRI = 11.13, P = 0.0507 ± 0.0159), tapir (PCRI = 11.13, P = 0.0469 ± 0.0118), elephant (PCRI = 10.7, P = 0.0787 ± 0.0195) and Malayan porcupine (Hystrix brachyura) (PCRI = 10.7, P = 0.103 ± 0.0252) were the common species utilising the crossing structures. In contrast, the Asian palm civet (Paradoxurus hermaphroditus) and leopard cat (Prionailurus bengalensis) were the most frequently hit species on the road [F(7,398) = 28.53, p < 0.0005]. The present study found that large-mammal species were utilising the crossing structures at a higher frequency, whereas more medium-mammal species were involved in traffic collisions.
... Factors including the lack of habitat enrichment activity, essential sources, and other physical factors might cause elephants' avoidance of the bridges. The frequent presence of elephants on the East-West Highway (Wadey et al., 2018;Wong et al., 2018b) and the placement of warning signages for elephants on the road (Timbuong, 2019) show a high tendency for this species to not using the CS. On the other hand, the viaducts were explicitly designed to connect the elephants' main landscapes (Saaban et al., 2011). ...
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