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Physiological stress responses in wild Asian elephants Elephas maximus in a

human-dominated landscape in the Western Ghats, southern India

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DOI: 10.1016/j.ygcen.2018.05.009

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Research paper

Physiological stress responses in wild Asian elephants Elephas maximus in a

human-dominated landscape in the Western Ghats, southern India
⁎
Sreedhar Vijayakrishnana,b,d, , Mavatur Ananda Kumarb, G. Umapathyc, Vinod Kumarc,
Anindya Sinhab,d,e
a
Postgraduate Programme in Wildlife Biology and Conservation, Wildlife Conservation Society – India Program and National Centre for Biological Sciences, Bangalore,
India
b
Nature Conservation Foundation, Mysore, India
c
Laboratory for the Conservation of Endangered Species, Centre for Cellular and Molecular Biology, Hyderabad, India
d
National Institute of Advanced Studies, Bangalore, India
e
Indian Institute of Science Education and Research, Kolkata, India

A R T I C LE I N FO A B S T R A C T

Keywords: Increasing anthropogenic pressures on forests, especially in the tropical regions of the world, have restricted
Asian elephant several large mammalian species such as the Asian elephant to fragmented habitats within human-dominated
Stress landscapes. In this study, we assessed the effects of an anthropogenic landscape and its associated conflict with
Behaviour humans on the physiological stress responses displayed by Asian elephants in the Anamalai Hills of the Western
Physiology
Ghats mountains in south India. We have quantified faecal glucocorticoid metabolite (FGM) concentrations in
Individual variation
focal individual elephants within and across herds, inhabiting both anthropogenic and natural habitats, and
Human-dominated landscape
evaluated their physiological responses to different socio-ecological situations between November 2013 and
April 2014. Physiological stress responses varied significantly among the tested elephant age- and sex categories
but not across different types of social organisation. Adults generally showed higher FGM concentrations, even in
the absence of stressors, than did any other age category. Males also appeared to have higher stress responses
than did females. Although there was no significant variation in mean stress levels between elephants on the
plateau in the absence of human interactions and those in adjacent, relatively undisturbed forest habitats, FGM
concentrations increased significantly for adult and subadult individuals as well as for calves following drives,
during which elephants were driven off aggressively by people. Our study emphasises the general importance of
understanding individual variation in physiology and behaviour within a population of a seriously threatened
mammalian species, the Asian elephant, and specifically highlights the need for long-term monitoring of the
stress physiology and behavioural responses of individual elephants across both human-dominated and natural
landscapes. Such studies would not only provide comprehensive insights into the adaptive biology of elephants
in changing ecological regimes but also aid in the development of effective management and conservation
strategies for endangered populations of the species.

1. Introduction
Growing demands for land resources globally have led to rapid
large-scale conversion of natural habitats into persistently expanding
anthropogenic landscapes (Balmford et al., 2003). Due to intense
modification of forestlands, several mammalian species, including
Asian elephants, have either lost or extended their ranges beyond their
native habitats into human-dominated landscapes. This has led to fre-
quent interactions with humans, often negative, widely referred to as
human-wildlife conflict (Graham et al., 2009; Kumar et al., 2010;
Athreya et al., 2013). Such modifications also demand that the affected
populations either adapt to these altered habitat conditions or be
eliminated from that particular habitat altogether. Apart from the evi-
dent effects of human-wildlife conflict such as crop- or property damage
and the loss of both human and animal lives, there are also hidden
impacts that can profoundly influence the well being of both humans
and the affected species (Fernando et al., 2012; Barua et al., 2013).
While there has been substantial research on the impact of such conflict
on humans, an understanding of the problems faced by the wild species
has been gaining momentum only in recent years, providing insights

⁎
Corresponding author at: National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560012, India.
E-mail address: sreedhar@ncf-india.org (S. Vijayakrishnan).

https://doi.org/10.1016/j.ygcen.2018.05.009
Received 18 December 2017; Received in revised form 11 April 2018; Accepted 7 May 2018
0016-6480/ © 2018 Elsevier Inc. All rights reserved.

Please cite this article as: Vijayakrishnan, S., General and Comparative Endocrinology (2018), https://doi.org/10.1016/j.ygcen.2018.05.009
S. Vijayakrishnan et al.
into the nature of responses shown by the taxa and their underlying
coping mechanisms (Cooke et al., 2013). This often involves the ac-
quisition of certain adaptive behavioural traits in particular situations
and even adaptation of physiological processes in response to the
nature and intensity of human disturbances (Atwell et al., 2012). Such
behavioural and physiological responses are usually critical for in-
dividuals to cope with changing environments, ensuring their long-term
survival and fitness (Tuomainen and Candolin, 2011).
Animal physiological adaptations to anthropogenic perturbations
such as tourism, poaching, vehicular traffic and other forms of conflict
have been investigated in a wide range of taxa, including birds (Atwell
et al., 2012), marmots (Smith et al., 2012), chipmunks (Martin and
Réale, 2008), elks (Ciuti et al., 2012a,b), lions (Creel et al., 2013) and
primates (Maréchal et al., 2011; Muehlenbein et al., 2012). In long-
lived species such as elephants with extended inter-calving periods, any
change in their physiological states, brought about by chronic stress,
could be detrimental to their survival and reproduction. The stress
physiology of African elephants, for example, has been well studied in
various contexts of human interactions (Foley et al., 2001; Gobush
et al., 2008; Munshi-South et al., 2008; Ahlering et al., 2011, 2013;
Jachowski et al., 2012, 2013; Tingvold et al., 2013). The effect of
conflict on the behaviour and physiology of Asian elephants, however,
remains relatively unexplored. A few studies have documented reduc-
tion in Asian elephant home ranges in conflict-prone areas
(Balasubramanian et al., 1995), sex-specific crop-raiding patterns
(Sukumar and Gadgil, 1988; Sukumar 1991), and change in time-ac-
tivity budgets and habitat use in relation to human disturbances
(Srinivasaiah et al., 2012). Considering the extent of habitat fragmen-
tation and escalated levels of human-elephant conflict in Asia, a more
comprehensive understanding of the behavioural and physiological
responses of Asian elephants to anthropogenic stressors in modified
landscapes is critical, not only for insights into their biology but also to
develop effective management strategies for affected populations.
In this study, we examined the physiological responses of a popu-
lation of Asian elephants Elephas maximus that interact regularly and
often intensely with local human communities in the human-modified
landscape of Anamalai hills in the Western Ghats of southern India, an
important conservation area for the species. We hypothesised that the
faecal glucocorticoid metabolite levels in elephants, living in such an
anthropogenic landscape, would be elevated in comparison to that in
individuals living in a relatively undisturbed, contiguous forest area
and also vary in individuals of different age-sex categories or social
organisations across these natural and modified habitats.
2. Methods
We conducted this study on the Valparai plateau and the neigh-
bouring Vazhachal Reserved Forest in the Anamalais Hills of the
Western Ghats, southern India, which is home to the second largest
contiguous Asian elephant population across its entire distributional
range (Fig. 1). The plateau is now a 220-km2 matrix of tea, coffee and
cardamom plantations, juxtaposed with rainforest fragments and Eu-
calyptus patches. Situated at an altitudinal range of 900–1450 m, the
natural vegetation of the plateau is classified as mid-elevation tropical
wet evergreen forest of the Cullenia-Mesua-Palaquium Type (Pascal
1988). About 80–100 elephants use the landscape annually, with this
population being tracked fairly regularly since 2002, as part of a larger
monitoring programme (Kumar et al., 2010). Frequent interactions
with humans, while moving through plantations, have often led to
human-elephant conflict, some of these events often terminating in
‘elephant drives’, during which the elephants are actively driven away
by people with the help of loud noise and heavy vehicles.
The Vazhachal Reserved Forest is an undisturbed evergreen habitat,
contiguous with the Anamalai Tiger Reserve, including the Valparai
plateau. A part of this forest serves as a buffer zone for the adjoining
Parambikulam Tiger Reserve. The vegetation typically consists of
2
General and Comparative Endocrinology xxx (xxxx) xxx–xxx
Ochlandra-dominated evergreen patches with intervening large open
swamps and grasslands, which support large numbers of ungulate
species such as sambar Rusa unicolor and gaur Bos gaurus, besides ele-
phant herds.
2.1. Study population
The study elephants, consisting of 69 individuals that were either in
mixed-sex herds, an all-male group or solitary (see Supplementary
Material), formed part of the 100-odd elephants that inhabit the pla-
teau; of these, 40–50 individuals have been reported to use the area
extensively for about nine months in a year (Kumar et al., 2010). Out of
the 69 study elephants, 33 were adults, 14 subadults, 11 juveniles,
while 11 were calves.
The study mixed-sex herds were identified on the basis of their
constituent females and all the study individuals, whether solitary or in
herds or the all-male group, by their characteristic morphological fea-
tures, including ear folds, tusk- and tail patterns, and old injury marks
on the body (Goswami et al., 2007). The group size and composition of
the study associations remained stable throughout the study period
except when solitary adult and subadult males joined these herds or the
all-male group for short periods of time or when the herds temporarily
divided into sub-herds following drives. All the six adult males
(age > 15 years), followed during the study period, were observed to
associate with one or more of these herds. These independently-moving
bulls have been considered as solitary males in all group-level analyses.
There was only a single solitary female on the Valparai plateau during
the study period.
The locations of the study herds were monitored on a daily basis
during the study period, as part of the above-mentioned ongoing ele-
phant-monitoring programme on the Valparai plateau. The herds and
solitary individuals were mostly tracked on foot or by using a four-
wheel vehicle.
2.2. Sample collection and metabolite extraction
We collected 5–10 g of fresh faecal samples from identified focal
individuals, whether in herds, all-male group or solitary, 36–48 h after
every session of observations conducted on them, either in the absence
of drives or after drives had been conducted. The samples were col-
lected after mixing each bolus thoroughly, to ensure a uniform dis-
tribution of the metabolites to be assayed across the dung pile. The
window of inference was optimised, based on the gut-retention time of
elephants, as known from an earlier study (Laws et al., 2007). The
collected samples were dried on the day of collection, using a blower-
heater setup for dry storage, a technique standardised for the field
(Hunt and Wasser 2003; Kumar et al., 2014).
Cortisol metabolite extraction was conducted in the laboratory
using procedures described by Kumar et al., (2014). The samples were
pulverised, sieved and 0.2 g of the resulting powder transferred to 15-
ml Falcon tubes; 80% methanol was then added and the mixture vor-
texed for 20 min. The samples were then centrifuged at 4000 rpm for
20 min and the supernatant solution refrigerated overnight at −20 °C.
Glucocorticoid metabolites were then extracted and isolated using a
cortisol polyclonal antibody (R4866) diluted to 1:9000, HRP-con-
jugated cortisol diluted to 1:250,000 and cortisol standards
(1000–1.95 pg/well) (Kumar et al., 2014). The plates for the enzyme-
linked immunosorbent assay (ELISA) were coated with the antibody
and refrigerated for about 12–16 h. The plates were then washed with a
washing buffer, horseradish peroxidase added and incubated for 2 h at
room temperature. Tetramethyl benzidine/hydrogen peroxide was then
added to the wells and incubated in the dark for 10–15 min. Finally, 1 N
hydrochloric acid was added and the samples analysed by an ELISA
reader. Known amounts of 3H-labelled steroids were added to the
samples prior to extraction to assess extraction efficiency (Umapathy
et al., 2013).
S. Vijayakrishnan et al.
Fig. 1. Map showing the matrix of rainforest fragments and monoculture plantations on the Valparai plateau, the adjoining protected areas and riverine networks in
southwestern India.
The intra- and inter-assay values for the coefficient of variation (CV)
were calculated as per Kumar et al. (2014) and found to be 2.98 and
5.30% respectively. The mean recovery percentage ( ± SD) of cortisol
from the faecal samples was estimated to be 84.65 ( ± 4.50)%.
A total of 298 samples, with a mean ( ± SE) of 4.31 ( ± 0.43) were
collected from the 69 identified individuals, with the number of sam-
ples per individual varying from 1 to 16. The total number of samples in
the absence of drives was 170 and that collected following drives were
128.
2.3. Statistical analyses
Analyses were carried out using the software R 3.0.1 (R Core
Development and Team, 2013). We used the non-parametric Kruskal-
Wallis test and Mann-Whitney U test to assess differences in the pro-
portion of time spent in different habitats by individual elephants, who
were either solitary or in herds or the all-male group, and in their
physiological stress responses, including mean faecal glucocorticoid
metabolite (FGM) concentrations.
To analyse the influence of drives on FGM concentrations, we used
data from only 47 individuals, for whom we had samples in the absence
of drives and following drives (n = 245; 123 samples collected in the
absence of and 122 following drives).
We used eleven candidate hierarchical linear mixed-effect models to
assess the factors influencing FGM concentrations in the study ele-
phants under different circumstances. The models were built using the
package lme4 in R (Bates et al., 2014). Age- and sex categories of ele-
phants as well as the occurrence of drives were taken as fixed effects.
The observed variation across individuals was accounted for as random
effects. Log-transforming the response variable ensured normality.
Model selection was based on Akaike’s Information Criterion while
model averaging was carried out using the package MuMIn in R (Barton,
2014) when considering competing models.
3
General and Comparative Endocrinology xxx (xxxx) xxx–xxx
3. Results
The mean faecal glucocorticoid metabolite (FGM) concentrations
per individual varied from 0.45 to 18 ng/g
(mean ± SE = 3.09 ± 0.14 ng/g) in the study individuals, which in-
cluded four mixed-sex herds, one all-male group, six solitary males and
a solitary female on the human-dominated Valparai plateau and one
herd in the peripheral, relatively undisturbed forests of Vazhachal. Two
outlying values of 35.25 and 48 ng/g, observed in a juvenile male and
an adult female respectively, were eliminated from further analyses as
the faecal samples collected from the same individuals on the previous
and the following days did not show any elevated levels and moreover,
there were no observed case of negative human interaction on the day
corresponding to these high FGM levels.
The mean FGM concentrations, displayed by the study elephants in
the absence of human interactions on the plateau, were not significantly
different from those of Vazhachal (Kruskal-Wallis test, χ2 = 7, df = 7,
p = 0.43). The mean FGM value of the all-male group was, however,
higher than that of the herds or of the solitary individuals.
The overall mean FGM levels in the study elephants were sig-
nificantly higher following elephant drives than were the mean baseline
values in the absence of such drives on the Valparai plateau (Mann-
Whitney U test; males: U = 885, n = 51 and 46, p = 0.03; females:
U = 2160, n = 72 and 76, p = 0.02; Fig. 2). Between the sexes, how-
ever, males tended to have relatively higher FGM concentrations (with
an increase of 40.84% of their baseline values) than did females
(20.89% increase) following such drives (U = 1555.5, n = 46 and 76,
p = 0.31).
The mean baseline FGM concentrations were the highest in adults
among the four age classes, followed by that in juveniles, subadults and
calves (Fig. 2). The magnitude of these values, however, changed dif-
ferently across the age categories following drives, with calves ex-
hibiting the highest increase (105.69%) over that of the subadults
(54.72%) or adults (24.14%). Juveniles, in contrast, exhibited a negli-
gible change in FGM concentrations, decreasing approximately 0.066%
S. Vijayakrishnan et al. General and Comparative Endocrinology xxx (xxxx) xxx–xxx

Fig. 2. Mean faecal glucocorticoid metabolite (FGM) concentrations in the study elephants across age classes, in the absence of and following drives. n = 245
matched samples, drawn from 47 individuals.

following drives. and individuals to move out of their natural environments and require
We tested 11 candidate hierarchical linear mixed-effect models to them to adapt behaviourally and physiologically to the changing eco-
examine the influence of age-and sex categories, and drive operations logical conditions (Tuomainen and Candolin, 2011; Atwell et al., 2012;
on FGM concentrations in the study elephants. Of these, three models Sol et al., 2013). Living in close proximity to humans and occasionally
competed fairly strongly and hence, model averaging was performed engaging in conflict with them could involve potential costs for many
(Table 1). The model-averaged coefficients indicated that all three nonhuman species in terms of forage availability, alteration (mostly
predictor variables—the occurrence of drives, age- and sex classes—- restriction) in ranging patterns, reproductive fitness and long-term
determined FGM levels, with an additive effect of the three variables survival for many species (Creel et al., 2002; Ciuti et al., 2012a,b). This
contributing to the observed stress levels in the study elephants (Fig. 3). is particularly true for the elephant as well, a large-bodied, long-ran-
ging mammalian species that typically requires extensive home ranges
4. Discussion to meet its foraging and other survival demands. Our study elephants
typically spend a significant proportion of their time annually within
Increasing anthropogenic pressures often coerce animal populations the tea, coffee and cardamom plantations on the Valparai plateau
(Kumar et al., 2010), where they regularly interact with people. An
Table 1 earlier study from the plateau indicated that the presence of people and
Model-averaged coefficients showing parameter estimates, including those of their proximity negatively influenced the behavioural responses of
age- and sex categories, drives and their interactions, which could potentially elephants, as measured by their reduced foraging time and elevated
influence FGM concentrations in the study elephants. proportions of time spent on alert behaviours (Kumar and Singh, 2010).
Model-averaged coefficients However, our study indicates that the faecal glucocorticoid metabolite
(FGM) concentrations of elephants on the human-dominated Valparai
Estimate Adjusted SE z value Pr(> |z|) plateau being comparable to those in the adjacent, undisturbed forest
habitats could be attributed to their being habituated to being in
Intercept 0.3957 0.0331 11.939 < 2e−16
DriveY 0.0929 0.0371 2.503 0.012
proximity with people and the resultant regular interactions with them.
AgeCalf −0.3707 0.1114 3.328 0.001
AgeJuvenile −0.2348 0.0747 3.143 0.001
AgeSubadult −0.1597 0.0619 2.58 0.009 4.1. Sociality and physiological stress responses
SexMale 0.1929 0.0601 3.209 0.001
AgeCalf:DriveY 0.2419 0.1530 1.581 0.113
AgeJuvenile:DriveY −0.0701 0.0954 0.735 0.462 Social structure, in terms of size and composition of a group, can
AgeSubadult:DriveY 0.0703 0.0818 0.859 0.390 significantly influence stress responses displayed by particular in-
DriveY:SexMale 0.0449 0.0716 0.628 0.530 dividuals (Creel et al., 2013). Social buffering in larger groups can, for
AgeJuvenile:SexMale −0.0174 0.1560 0.112 0.910 example, reduce stress, as has been reported in certain mammalian taxa
AgeSubadult:SexMale −0.0926 0.1182 0.783 0.433
(Alberts et al., 1992; Creel et al., 2013). Although Asian elephants are
AgeJuvenile:DriveY:SexMale −0.4288 0.2602 1.648 0.099
AgeSubadult:DriveY:SexMale −0.1353 0.2061 0.657 0.511 believed to have fission-fusion societies (de Silva and Wittemyer, 2012),
the herds in the study region were more or less stable throughout the

4
S. Vijayakrishnan et al. General and Comparative Endocrinology xxx (xxxx) xxx–xxx

Fig. 3. Parameter estimates of all variables included in the hierarchical linear model, showing the influence of elephant drives on stress responses across age classes
(with 95% confidence intervals calculated from the SE).

duration of the study in terms of their group size and composition, and individual with high FGM levels did not show these particular stages of
we did not, therefore, as expected, observe any influence of these de- musth but exhibited other signs, such as touching the trunk to the head,
mographic parameters on the physiological stress responses of our scratching the temporal gland against a tree, musth walk and ear wave
study elephants. (Poole, 1987). The literature on African and Asian elephants reveals
that musth is not necessarily associated with elevated glucocorticoid
levels (Ganswindt et al., 2003; Ahlering et al., 2011; Ghosal et al.,
4.2. Habituation and physiological stress responses
2013). Our results, however, warrant a close examination of individual
variation in the possible association of musth with physiological stress
It is perhaps noteworthy that, on the Valparai plateau, except the
responses, both within and across populations. Importantly, the study
all-male group, the study elephants appeared to be physiologically
also suggests that elevated levels of FGM may not always be associated
adapted to anthropogenic habitats, in terms of their stress response,
with the high risks invoked by human-elephant conflict, as noticed in
particularly in the absence of direct antagonistic interactions. This was
African elephants (Ahlering et al., 2011). On the Valparai plateau, adult
evidenced by the baseline FGM levels of the elephants on the human-
males are rarely associated with human conflict and damage to prop-
dominated Valparai plateau, which, as pointed out above, were com-
erty or lives, unlike their female counterparts (pers. obs.).
parable to that of the individuals in the relatively undisturbed
Although there is no clear evidence yet, it is possible that the re-
Vazhachal Reserved Forest. Plantations on the Valparai plateau were
latively high baseline FGM concentrations displayed by adult males
established about a century ago, and subsequent use of the area by
could primarily be attributed to their solitary nature; they also, gen-
humans have led to their regular interactions with elephants, often
erally, exhibited relatively higher physiological stress-induced hor-
resulting in conflict (Congreve, 1942), but also possibly leading to the
mones, as compared to females. There could, nevertheless, be multiple
habituation of elephants to the human-use landscape.
factors that potentially affect stress levels in males and female ele-
The average glucocorticoid metabolite levels displayed by females
phants, including their social dynamics, reproductive status, forage
in Valparai, in the absence of intense human interactions such as drives,
availability and season (Creel 2001; Sapolsky 2005; Ahlering et al.,
appear to be less than captive female Asian elephants living under re-
2011; Baker et al., 2013). We acknowledge the limitations of our study,
stricted environmental and space conditions (Kumar et al., 2014). The
as it covered only one season and did not offer us opportunities to
adult males in the study population, however, showed relatively higher
observe the influence of social status, forage availability or nutritional
FGM concentrations than did females, a finding that corroborates with
status, as measured by the body condition index (Fernando and Janaka,
earlier studies on free-ranging male African elephants (Ahlering et al.,
2009; Pokharel et al., 2017), on individual elephants, male or female,
2011; Tingvold et al., 2013) or on male Asian elephants in captivity
during the study period. Our study, thus, highlights the importance of
(Kumar et al., 2014). Of the six adult male elephants that we in-
long-term studies on the stress responses of elephants, both behavioural
vestigated, two displayed symptoms of musth and had high FGM con-
and physiological, in the future.
centrations. One of them was observed to be in musth (temporal-gland-
The average glucocorticoid levels in adult elephants were higher
secretion and urine-dribbling stage; Rasmussen and Perrin 1999) on one
than those shown by the other age classes although the magnitude of
occasion and in post-musth on another while the other was sampled
increase following drives was relatively lower. This suggests that,
once and was in musth (temporal-gland-secretion stage). Yet another

5
S. Vijayakrishnan et al.
having spent a greater part of their lifetime in a human-dominated
landscape, the adults may have now habituated to various perturba-
tions unless they face serious forms of reactive interactions, such as the
bursting of crackers or being chased away. On the other hand, calves
appeared to respond strongly to stressors such as drives, possibly due to
a relative lack of exposure to such conflict. The relatively high FGM
baselines in adults, particularly females, could be due to the presence of
calves and juveniles in the herd and the risks associated with human-
dominated landscapes (Ahlering et al., 2011). Exploring the important
role that life-history parameters may play in defining physiological
responses to stress in Asian elephants is an imperative, given the need
to formulate management strategies for elephant populations such as
our own.
This study, we strongly believe, encourages the need to understand
the variability in stress responses across individual Asian elephants,
especially in populations that are increasingly facing elevated levels of
negative interactions with people. The solitary female in the study area
showed significantly elevated glucocorticoid metabolite levels as com-
pared to other female elephants, both in the absence of and during
intense interactions with humans. This could once again possibly be
attributed, as in the case of the adult males, to her solitary nature, an
unusual situation for highly sociable female elephants with strong kin
relationships (Gobush et al., 2008). These observations thus highlight
the critical importance of social buffering as a potential stress-coping
mechanism that could aid individual elephants in mixed-sex herds in
otherwise stressful ecological and behavioural situations.
5. Conclusions
A comprehensive understanding of the behavioural and physiolo-
gical responses displayed by individual animals to stress-inducing sti-
muli in altered environments could contribute significantly to addres-
sing conservation problems, especially that of highly threatened taxa
(Cooke and O’Connor, 2010). This study highlights the importance of
human interactions in inducing physiological stress responses in a po-
pulation of Asian elephants, as revealed by their elevated faecal glu-
cocorticoid metabolite levels. We, therefore, suggest that, for large
endangered species such as elephants, an understanding of individual
physiological responses is critical for the development of sustainable
management and conservation strategies, a feature virtually overlooked
in elephant conservation practices today. Proactive steps, such as dis-
couraging elephant drives, minimising human-induced disturbances or
facilitating the free movement of elephants could help reduce stress in
affected populations in increasingly altered landscapes. Our study also
indicates the need for understanding the behavioural correlates of
physiological stress in order to facilitate the long-term monitoring and
conservation of elephant populations in modified landscapes.
Acknowledgements
The study was supported by a grant from the Department of Science
and Technology, Government of India, to the National Centre for
Biological Sciences. We wish to thank the National Centre for Biological
Sciences, Wildlife Conservation Society – India Program, Nature
Conservation Foundation, and the Laboratory for Conservation of
Endangered Species for supporting this work. We acknowledge the
Tamil Nadu and Kerala State Forest Departments for granting permits
for our fieldwork. We are grateful to Ajith Kumar, Jayashree Ratnam,
Divya Mudappa and T R Shankar Raman for their encouragement as
well as helpful suggestions and comments on earlier versions of this
manuscript. We acknowledge the logistical support provided by
Chandni Gurusrikar, Ganesh Raghunathan and Aneesh S. We would
also like to thank two anonymous reviewers for their critical and con-
structive comments, which helped improve the manuscript sub-
stantially.
6
General and Comparative Endocrinology xxx (xxxx) xxx–xxx
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the
online version, at https://doi.org/10.1016/j.ygcen.2018.05.009.
References
Ahlering, M.A., Millspaugh, J.J., Woods, R.J., Western, D., Eggert, L.S., 2011. Elevated
levels of stress hormones in crop-raiding male elephants. Anim. Conserv. 14,
124–130.
Ahlering, M.A., Maldonado, J.E., Eggert, L.S., Fleischer, R.C., Western, D., Brown, J.L.,
2013. Conservation outside protected areas and the effect of human-dominated
landscapes on stress hormones in savannah elephants. Conserv. Biol. 27, 569–575.
Alberts, S.C., Sapolsky, R.M., Altmann, J., 1992. Behavioral, endocrine, and im-
munological correlates of immigration by an aggressive male into a natural primate
group. Horm. Behav. 26, 167–178.
Athreya, V., Odden, M., Linnell, J.D.C., Krishnaswamy, J., Karanth, U., 2013. Big cats in
our backyards: persistence of large carnivores in a human dominated landscape in
India. PLoS ONE 8, 2–9.
Atwell, J.W., Cardoso, G.C., Whittaker, D.J., Campbell-Nelson, S., Robertson, K.W.,
Ketterson, E.D., 2012. Boldness behavior and stress physiology in a novel urban
environment suggest rapid correlated evolutionary adaptation. Behav. Ecol. 23,
960–969.
Baker, M.R., Gobush, K.S., Vynne, C.H., 2013. Review of factors influencing stress hor-
mones in fish and wildlife. J. Nat. Conserv. 21, 309–318.
Balasubramanian, M., Bhaskaran, N., Swaminathan, S., Desai, A.A., 1995. Crop raiding by
Asian elephants (Elephas maximus) in the Nilgiri Biosphere Reserve, South India. In:
Daniel, J.C., Datye, H.S. (Eds.), A week with elephants. Bombay Natural History
Society, Oxford University, Bombay, India, pp. 350–367.
Balmford, A., Green, R.E., Jenkins, M., 2003. Measuring the changing state of nature.
Trends Ecol. Evol. 18, 326–330. http://dx.doi.org/10.1016/S0169-5347(03)
00067-3.
Barton, K., 2014. Mumin: Multi model inference. Version 1.10.0 1–46. https://CRAN.R-
project.org/package=MuMIn.
Barua, M., Bhagwat, S.A., Jadhav, S., 2013. The hidden dimensions of human–wildlife
conflict: health impacts, opportunity and transaction costs. Biol. Conserv. 157,
309–316.
Bates, D., Martin, M., Bolker, B., and Walker, S., 2014. lme4: Linear mixed-effects models
using Eigen and S4. R package version 1.1-6. http://CRAN.R-project.org/package=
lme.
Ciuti, S., Northrup, J.M., Muhly, T.B., Simi, S., Musiani, M., Pitt, J.A., Boyce, M.S., 2012a.
Effects of humans on behaviour of wildlife exceed those of natural predators in a
landscape of fear. PLoS ONE 7, e50611.
Ciuti, S., Muhly, T.B., Paton, D.G., McDevitt, A.D., Musiani, M., Boyce, M.S., 2012b.
Human selection of elk behavioural traits in a landscape of fear. Proc. R. Soc. B Biol.
Sci. 279, 4407–4416.
Congreve, H.R.T., 1942. The Anamalais. Associated Printers, Madras (now Chennai).
Cooke, S.J., O’Connor, C.M., 2010. Making conservation physiology relevant to policy
makers and conservation practitioners. Conserv. Lett. 3, 159–166.
Cooke, S.J., Sack, L., Franklin, C.E., Farrell, A.P., Beardall, J., Wikelski, M., Chown, S.L.,
2013. What is conservation physiology? Perspectives on an increasingly integrated
and essential science. Conserv. Physiol. 1, 1–23.
Creel, S., 2001. Social dominance and stress hormones. Trends Ecol. Evol. 16, 491–497.
Creel, S., Fox, J.E., Hardy, A., Sands, J., Garrott, B., Peterson, R.O., 2002. Snowmobile
activity and glucocorticoid stress responses in wolves and elks. Conserv. Biol. 16,
809–814.
Creel, S., Dantzer, B., Goymann, W., Rubenstein, D.R., 2013. The ecology of stress: effects
of the social environment. Funct. Ecol. 27, 66–80.
de Silva, S., Wittemyer, G., 2012. A comparison of social organization in Asian elephants
and African savannah elephants. Int. J. Primatol. 33, 1125–1141.
Fernando, P., Janaka, H., 2009. A simple method for assessing elephant body condition.
Gajah 31, 29–31.
Fernando, P., Leimgruber, P., Prasad, T., Pastorini, J., 2012. Problem-elephant translo-
cation: Translocating the problem and the elephant? PLoS ONE 7, e50917.
Foley, C.A.H., Papageorge, S., Wasser, S.K., 2001. Noninvasive stress and reproductive
measures of social and ecological pressures in free ranging African elephants.
Conserv. Biol. 15, 1134–1142.
Ghosal, R., Ganswindt, A., Seshagiri, P.B., Sukumar, R., 2013. Endocrine correlates of
musth in free-ranging Asian elephants (Elephas maximus) determined by non-invasive
faecal steroid hormone metabolite measurements. PLoS ONE 8, e84787.
Gobush, K.S., Mutayoba, B.M., Wasser, S.K., 2008. Long-term impacts of poaching on
relatedness, stress physiology, and reproductive output of adult female African ele-
phants. Conserv. Biol. 22, 1590–1599.
Goswami, V.R., Madhusudan, M.D., Karanth, K.U., 2007. Application of photographic
capture-recapture modelling to estimate demographic parameters for male Asian
elephants. Anim. Conserv. 10, 391–399.
Graham, M.D., Douglas-Hamilton, I., Adams, W.M., Lee, P.C., 2009. The movement of
African elephants in a human-dominated land-use mosaic. Anim. Conserv. 12,
445–455. http://dx.doi.org/10.1111/j.1469-1795.2009.00272.x.
Hunt, K.E., Wasser, S.K., 2003. Effect of long-term preservation methods on fecal glu-
cocorticoid concentrations of grizzly bear and African elephant. Physiol. Biochem.
Zool. 76, 918–928.
Jachowski, D.S., Slotow, R., Millspaugh, J.J., 2012. Physiological stress and refuge be-
havior by African elephants. PLoS ONE 7, e31818.
S. Vijayakrishnan et al.
Jachowski, D.S., Montgomery, R.A., Slotow, R., Millspaugh, J.J., 2013. Unravelling
complex associations between physiological state and movement of African ele-
phants. Funct. Ecol. 27, 1166–1175.
Kumar, M.A., Singh, M., 2010. Behavior of Asian elephant (Elephas maximus) in a land-use
mosaic: implications for human-elephant coexistence in the Anamalai Hills, India.
Wildl. Biol. Pract. 6, 69–80.
Kumar, M.A., Mudappa, D., Shankar Raman, T.R., 2010. Asian elephant Elephas maximus
habitat use and ranging in fragmented rainforest and plantations in the Anamalai
Hills, India. Tropical Conserv. Sci. 33, 143–158.
Kumar, V., Palugulla Reddy, V., Kokkiligadda, A., Shivaji, S., Umapathy, G., 2014. Non-
invasive assessment of reproductive status and stress in captive Asian elephants in
three south Indian zoos. Gen. Comp. Endocrinol. 201, 37–44.
Laws, N., Ganswindt, A., Heistermann, M., Harris, M., Harris, S., Sherwin, C., 2007. A case
study: fecal corticosteroid and behavior as indicators of welfare during relocation of
an Asian elephant. J. Appl. Anim. Welf. Sci. 10, 349–358.
Maréchal, L., Semple, S., Majolo, B., Qarro, M., Heistermann, M., MacLarnon, A., 2011.
Impacts of tourism on anxiety and physiological stress levels in wild male Barbary
macaques. Biol. Conserv. 144, 2188–2193.
Martin, J.G.A., Réale, D., 2008. Animal temperament and human disturbance: implica-
tions for the response of wildlife to tourism. Behav. Processes 77, 66–72.
Muehlenbein, M.P., Ancrenaz, M., Sakong, R., Ambu, L., Prall, S., Fuller, G., Raghanti,
M.A., 2012. Ape conservation physiology: fecal glucocorticoid responses in wild
Pongo pygmaeus morio following human visitation. PLoS ONE 7, e33357.
Munshi-South, J., Tchignoumba, L., Brown, J., Abbondanza, N., Maldonado, J.E.,
Henderson, A., Alonso, A., 2008. Physiological indicators of stress in African forest
elephants (Loxodonta africana cyclotis) in relation to petroleum operations in Gabon,
Central Africa. Divers. Distrib. 14, 995–1003.
Pascal, J.P., 1988. Wet Evergreen Forests of the Western Ghats of India: Ecology,
Structure Floristic Composition and Succession. Institute Français de Pondichéry,
Pondicherry, India.
Pokharel, S.S., Seshagiri, P.B., Sukumar, R., 2017. Assessment of season-dependent body
View publication stats
General and Comparative Endocrinology xxx (xxxx) xxx–xxx
condition scores in relation to faecal glucocorticoid metabolites in free-ranging Asian
elephants. Conserv. Physiol. 5. http://dx.doi.org/10.1093/conphys/cox039.
Poole, J.H., 1987. Rutting behavior in African elephants: the phenomenon of musth.
Behaviour 102, 283–316.
R. Core Development Team, 2013. R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna.
Rasmussen, L.E., Perrin, T.E., 1999. Physiological correlates of musth. Physiol. Behav. 67,
539–549.
Sapolsky, R.M., 2005. The influence of social hierarchy on primate health. Science 308,
648–652.
Smith, J.E., Monclús, R., Wantuck, D., Florant, G.L., Blumstein, D.T., 2012. Fecal gluco-
corticoid metabolites in wild yellow-bellied marmots: experimental validation, in-
dividual differences and ecological correlates. Gen. Comp. Endocrinol. 178, 417–426.
Sol, D., Lapiedra, O., González-Lagos, C., 2013. Behavioural adjustments for a life in the
city. Anim. Behav. 85, 1101–1112.
Srinivasaiah, N.M., Anand, V.D., Vaidyanathan, S., Sinha, A., 2012. Usual populations,
unusual individuals: Insights into the behavior and management of Asian elephants in
fragmented landscapes. PLoS ONE 7, e42571.
Sukumar, R., 1991. The management of large mammals in relation to male strategies and
conflict with people. Biol. Conserv. 55, 93–102.
Sukumar, R., Gadgil, M., 1988. Male-female differences in foraging on crops by Asian
elephants. Anim. Behav. 36, 1233–1235.
Tingvold, H.G., Fyumagwa, R., Bech, C., Baardsen, L.F., Rosenlund, H., Røskaft, E., 2013.
Determining adrenocortical activity as a measure of stress in African elephants
(Loxodonta africana) in relation to human activities in Serengeti ecosystem. Afr. J.
Ecol. 51, 580–589.
Tuomainen, U., Candolin, U., 2011. Behavioural responses to human-induced environ-
mental change. Biol. Rev. 86, 640–657.
Umapathy, G., Kumar, V., Wasimuddin, Kabra, M., Shivaji, S., 2013. Detection of preg-
nancy and fertility status in big cats using an enzyme immunoassay based on 5α-
pregnan-3α-ol-20-one. Gen. Comp. Endocrinol. 180, 33–38.