Content uploaded by Salman Saaban
Author content
All content in this area was uploaded by Salman Saaban on Mar 21, 2020
Content may be subject to copyright.
See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/327763844
The Elephant who Finally Crossed the Road – Significant Life Events Reflected
in Faecal Hormone Metabolites of a Wild Asian Elephant
Article · September 2018
CITATIONS
0
READS
39
6 authors, including:
Some of the authors of this publication are also working on these related projects:
Management & Ecology of Malaysian Elephants View project
The Link between Knowledge, Attitudes and Practices in Relation to Atmospheric Haze Pollution in Peninsular Malaysia View project
Ee Phin Wong
University of Nottingham, Malaysia Campus
6 PUBLICATIONS10 CITATIONS
SEE PROFILE
Ahimsa Campos-Arceiz
University of Nottingham, Malaysia Campus
116 PUBLICATIONS982 CITATIONS
SEE PROFILE
Salman Saaban
Department of Wildlife & Nat. Parks Peninsular Malaysia
21 PUBLICATIONS60 CITATIONS
SEE PROFILE
Jamie Wadey
University of Nottingham, Malaysia Campus
11 PUBLICATIONS17 CITATIONS
SEE PROFILE
All content following this page was uploaded by Jamie Wadey on 20 September 2018.
The user has requested enhancement of the downloaded file.
4
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 – Signicant Life Events Reected 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 reective 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 identied 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 conict (HEC).
Translocation, moving elephants from conict
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 proles
(Wong 2017) of translocated and local resident
elephants at release sites. Here we present a case
study that uses movement tracking and hormone
proles 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 collar’s 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 coefcient 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 inuence
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) signicant life events can be reected in wild
elephants’ fGCM concentrations. Although our
sample size is too small to draw conclusions, our
Figure 3. Faecal glucocorticoid metabolites
prole 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.
References
Blake S & Hedges S (2004) Sinking the agship:
The case of forest elephants in Asia and Africa.
Conservation Biology 18: 1191-1202.
Brown JL (2000) Reproductive endocrine
monitoring of elephants: An essential tool for
assisting captive management. Zoo Biology 367:
347-367.
Busch DS & Hayward LS (2009) Stress
in a conservation context: A discussion of
glucocorticoid actions and how levels change
with conservation-relevant variables. Biological
Conservation 142: 2844-2853.
Chrousos GP (1998) Stressors, stress, and
neuroendocrine integration of the adaptive
response. The 1997 Hans Selye Memorial
Lecture. Annals of the New York Academy of
Sciences 851(April): 311-335.
Cicchetti D & Walker EF (2001) Editorial:
Stress and development : Biological and
psychological consequences. Development and
Psychopathology 13: 413-418.
Dickens MJ, Delehanty DJ & Romero LM
(2010) Stress: An inevitable component of
animal translocation. Biological Conservation
143: 1329-1341.
Dickens MJ, Delehanty DJ & Romero LM (2009)
Stress and translocation: Alterations in the stress
physiology of translocated birds. Proceedings
of the Royal Society B: Biological Sciences 276
(1664): 2051-2056.
Edwards LD, Heyman AH & Swidan S (2011)
Hypocortisolism: An evidence-based review.
Integrative Medicine 10 (4): 30-38.
Fernando P & Pastorini J (2011) Range-wide
status of Asian elephants. Gajah 35: 15-20.
Franklin TB, Russig H, Weiss IC, Gräff J, Linder
N, Michalon A, … Mansuy IM (2010) Epigenetic
transmission of the impact of early stress across
generations. Biology Psychiatry 68: 408-415.
Goymann W (2012) On the use of non-invasive
hormone research in uncontrolled, natural
environments: the problem with sex, diet,
metabolic rate and the individual. Methods in
Ecology and Evolution 3: 757-765.
Hedges S, Tyson MJ, Sitompul AF, Kinnaird MF
& Gunaryadi D (2005) Distribution, status, and
conservation needs of Asian elephants (Elephas
10
maximus) in Lampung Province, Sumatra,
Indonesia. Biological Conservation 124: 35-48.
Heim C, Ehlert U & Hellhammer DH (2000)
The potential role of hypocortisolism in the
pathophysiology of stress-related bodily dis-
orders. Psychoneuroendocrinology 25: 1-35.
Khan N, Peters RA, Richardson E & Robert KA
(2016) Maternal corticosterone exposure has
transgenerational effects on grand-offspring.
Biology Letters 12: e20160627.
Lee P & Ho KKY (2013) Acute adrenal crisis.
In: Acute Endocrinology: From Cause to
Consequence. Van den Berghe G (ed) Humana
Press, New York. Vol. 53, pp 1689-1699.
Linklater WL, MacDonald EA, Flamand JRB
& Czekala NM (2010) Declining and low fecal
corticoids are associated with distress, not accli-
mation to stress, during the translocation of
African rhinoceros. Animal Cons. 13: 104-111.
Madliger CL & Love OP (2014) The need for
a predictive, context-dependent approach to the
application of stress hormones in conservation.
Conservation Biology 28: 283-287.
Matthews SG & Phillips DI (2012) Trans-
generational inheritance of stress pathology.
Experimental Neurology 233: 95-101.
McEwen BS (1998) Stress, adaptation, and
disease. Allostasis and allostatic load. Annals of
the New York Academy of Sciences 840: 33-44.
McEwen BS, Bowles NP, Gray JD, Hill MN,
Hunter RG, Karatsoreos IN & Nasca C (2015)
Mechanisms of stress in the brain. Nature
Neuroscience 18: 1353-1363.
McEwen BS & Wingweld JC (2003) The
concept of allostasis in biology and biomedicine.
Hormones and Behavior 43: 2-15.
Millspaugh JJ & Washburn BE (2004) Use of
fecal glucocorticoid metabolite measures in
conservation biology research: Considerations
for application and interpretation. USDA National
Wildlife Research Center-Staff Publications 138
(Paper 395): 189-199.
Palme R, Rettenbacher S, Touma C, El-Bahr SM
& Möstl E (2005) Stress hormones in mammals
and birds: Comparative aspects regarding
metabolism, excretion, and noninvasive
measurement in fecal samples. Annals of the New
York Academy of Sciences 1040: 162-171.
Pawluski J, Jego P, Henry S, Bruchet A, Palme
R, Coste C & Hausberger M (2017) Low plasma
cortisol and fecal cortisol metabolite measures as
indicators of compromised welfare in domestic
horses (Equus caballus). PloS One 12: e0182257.
Raison CL & Miller AH (2003) When not
enough is too much: The role of insufcient
glucocorticoid signaling in the pathophysiology
of stress-related disorders. American Journal of
Psychiatry 160: 1554-1565.
Rayan DM & Linkie M (2015) Conserving tigers
in Malaysia: A science-driven approach for
eliciting conservation policy change. Biological
Conservation 184: 18-26.
Rees SL, Panesar S, Steiner M & Fleming
AS (2004) The effects of adrenalectomy and
corticosterone replacement on maternal behavior
in the postpartum rat. Hormones and Behavior
46: 411-419.
Saaban S, Othman N, Yasak NMB, Nor BM, Zar
A & Campos-Arceiz A (2011) Current status of
Asian elephants in Peninsular Malaysia. Gajah
35: 67-75.
Sapolsky RM (1999) Glucocorticoids, stress, and
their adverse neurological effects: Relevance to
aging. Experimental Gerontology 34: 721-732.
Sapolsky RM (2004) Why Zebras Don’t Get
Ulcers. Henry Holt and Company, New York.
Sapolsky RM, Romero LM & Munck, AU
(2000) How do glucocorticoids inuence stress
responses? Integrating permissive, suppressive,
stimulatory and preparative actions. Endocrine
Reviews 21: 55-89.
11
Selye H (1950) Stress and the general adaptation
syndrome. British Medical Journal (June 17) 1
(4667): 1383-1392.
Sheriff MJ, Dantzer B, Delehanty B, Palme R &
Boonstra R (2011) Measuring stress in wildlife:
Techniques for quantifying glucocorticoids.
Oecologia 166: 869-887.
Sheriff MJ, Kerbs CJ & Boonstra R (2010a)
Assessing stress in animal populations: Do fecal
and plasma glucocorticoids tell the same story?
General and Comparative Endocrinology 166:
614-619.
Sheriff MJ, Krebs CJ & Boonstra, R (2010b) The
ghost of predators past: Population cycles and the
role of maternal programming under uctuatin
predation risk. Ecology 91: 2983-2994.
Silverman MN, Pearce BD, Biron CA &
Miller AH (2005) Immune modulation of the
hypothalamic-pituitary-adrenal (HPA) axis
during viral infection. Viral Immunology 18: 41-
78.
Terborgh J, Davenport LC, Ong L & Campos-
Arceiz A (2017) Foraging impacts of Asian
megafauna on tropical rain forest structure and
biodiversity. Biotropica 50: 84-89.
Thiel D, Jenni-Eiermann S, Braunisch V,
Palme R & Jenni L (2008) Ski tourism affects
habitat use and evokes a physiological stress
response in capercaillie Tetrao urogallus: A new
methodological approach. Journal of Applied
Ecology 45: 845-853.
Touma C & Palme R (2005) Measuring fecal
glucocorticoid metabolites in mammals and
birds: the importance of validation. Annals of the
New York Academy of Sciences 1046: 54-74.
Vijayakrishnan, S, Mavatur, AK, Umapathy,
G, Kumar, V & Sinha, A (2018) Physiological
stress responses in wild Asian elephants Elephas
maximus in a human-dominated landscape in
the Western Ghats, southern India. General and
Comparative Endocrinology 266: 150-156.
Wadey J, Beyer HL, Saaban S, Othman N,
Leimgruber P & Campos-Arceiz A (2018) Why
did the elephant cross the road? The complex
response of wild elephants to a major road in
Peninsular Malaysia. Biological Conservation
218: 91-98.
Wasser SK, Bevis K, King G & Hanson E
(1997) Noninvasive physiological measures
of disturbance in the northern spotted owl.
Conservation Biology 11: 1019-1022.
Watson R, Munro C, Edwards KL, Norton V,
Brown JL & Walker SL (2013) Development of a
versatile enzyme immunoassay for non-invasive
assessment of glucocorticoid metabolites in a
diversity of taxonomic species. General and
Comparative Endocrinology 186: 16-24.
Wingweld JC & Kitaysky AS (2002) Endocrine
responses to unpredictable environmental events:
Stress or anti-stress hormones? Integrative and
Comparative Biology 42: 600-609.
Wong EP (2017) Non-Invasive Monitoring
of Stress in Wild Asian Elephants (Elephas
maximus) in Peninsular Malaysia. Ph.D. thesis,
University of Nottingham Malaysia.
Wong EP, Yon L, Purcell R, Walker SL,
Othman N, Saaban S & Campos-Arceiz A
(2016) Concentrations of fecal glucocorticoid
metabolites in Asian elephant’s dung are stable for
up to 8 h in a tropical environment. Conservation
Physiology 4: cow070.
Yamamoto-Ebina S, Saaban S, Campos-Arceiz
A & Takatsuki S (2016) Food habits of Asian
elephants Elephas maximus in a rainforest of
northern Peninsular Malaysia. Mammal Study
41: 155-161.
Yehuda R & Seckl J (2011) Minireview: Stress-
related psychiatric disorders with low cortisol
levels: A metabolic hypothesis. Endocrinology
152: 4496-4503.
View publication statsView publication stats