Vol.

21: 223–230, 2013 ENDANGERED SPECIES RESEARCH

Published online September 6
doi: 10.3354/esr00527 Endang Species Res

First parasitological survey of Endangered Bornean

elephants Elephas maximus borneensis
Stephanie Hing1,*, Nurzhafarina Othman2, 3, Senthilvel K. S. S. Nathan2, 4, Mark Fox5,
Matthew Fisher6, Benoit Goossens2, 3, 4
1
Department of Life Sciences, Imperial College London, London, UK
2
Organisms and Environment Division, School of Biosciences, Cardiff University, Cardiff, UK
3
Danau Girang Field Centre, Sabah Wildlife Department, Kota Kinabalu, Sabah, Malaysia
4
Sabah Wildlife Department, Kota Kinabalu, Sabah, Malaysia
5
The Royal Veterinary College, London, UK
6
Department of Infectious Disease Epidemiology, Imperial College London, London, UK

ABSTRACT: Relatively few studies have been carried out on the parasites of free-ranging wild
animal species, which has led to a lack of baseline parasitological data. This is a concern because
endoparasites can have an important influence on fitness and survival, particularly in small popu-
lations of endangered species. This field study is the first parasitological survey of Endangered
Bornean elephants Elephas maximus borneensis. Using a special modification of the McMaster
method, trematode, cestode and nematode ova were identified in the faeces of wild Bornean ele-
phants in 2 key range areas in Sabah, Malaysian Borneo: the Tabin Wildlife Reserve and the
Lower Kinabatangan Wildlife Sanctuary. Preliminary comparisons between the sites suggest that
prevalence, load and diversity vary between the two, leading to hypotheses on host, parasite and
environmental factors which may affect endoparasite infection dynamics in wild Bornean ele-
phants. This study provides an initial catalogue of parasite types in the Bornean elephant and
reports on endoparasite prevalence and load, valuable baseline data for future research.

KEY WORDS: Bornean elephant · Endoparasites · Trematode · Cestode · Nematode ·

Anoplocephala · Fasciola
Resale or republication not permitted without written consent of the publisher

INTRODUCTION Parasites are any organisms that live in or on a host,

deriving benefit at the expense of the host. For the
There is a dearth of baseline parasitology data avail- purposes of this study, the term ‘parasites’ is used to
able for wild animal species (Mathews 2009). Despite refer to endoparasites of the gastrointestinal tract and
the significance of parasites in wildlife population hepatobilliary system, for example, strongyle nema-
health, their relevance in conservation has generally todes and liver flukes. Parasites can shape presence,
been neglected (Gómez et al. 2012). The majority of absence, population size and viability either directly,
English language conservation textbooks published affecting host fecundity, morbidity and mortality, or
between 1970 and 2009 made no mention of parasites indirectly, for example, via host debility and influence
(Nichols & Gómez 2011). Calls are growing for re- on immunocompetence (Gulland 1995, Hechinger &
.search to improve our understanding of parasites in Lafferty 2005, Nichols & Gómez 2011). Giant panda, a
conservation because parasites can play an important flagship for wildlife conservation, provide a stark il-
role in ecosystem function, host evolution, fitness and lustration of how parasites can affect species survival.
survival, especially in small populations of endangered Currently, the most significant threat to wild panda is
species (Lafferty 1997, Gregory & Hudson 2000, nematode parasite infection (Zhang et al. 2008).
Marcogliese 2004, Whiteman & Parker 2005, Gillespie Parasites are also important in conservation as they
& Chapman 2006, Gómez et al. 2012, Suzan et al. 2012). can serve as a non-invasive warning system for

*Email: [email protected] © Inter-Research 2013 · www.int-res.com

224 Endang Species Res 21: 223–230, 2013

wildlife and habitat health because environmental

changes impact upon hosts, parasites and their shared
environment (Lafferty 1997, Marcogliese 2005). In
2012 for the very first time, a chapter in a conserva-
tion textbook was dedicated to links between habitat
loss, habitat fragmentation and infectious disease
ecology (Suzan et al. 2012). Habitat loss and frag-
mentation can affect infection dynamics via a variety
of mechanisms, including hindering animal move-
ment, impeding gene flow (Coulon et al. 2004), facil-
itating edge effects (Chapman et al. 2006a), introduc-
ing environmental contamination (Deem et al. 2001),
altering the ecology of intermediate hosts (Page et al.
2001), changing host population size and density
(Mbora & McPeek 2009), limiting nutrition (Chap-
man et al. 2006b), facilitating contact and conflict
with people (Nelson et al. 2003), and subjecting ani-
mals to psychological and physiological stress,
thereby affecting immunocompetence (McCallum &
Dobson 2002). Parasites have the potential to be used
as indicators of stress in wildlife threatened by habi-
tat fragmentation (Schwitzer et al. 2010).
The main threats to the survival of Bornean ele- Fig. 1. A wild Bornean elephant calf. Photo: Stephanie Hing
phants Elephas maximus borneensis (Fig. 1), and in-
deed Asian elephants E. maximus on the mainland,
are anthropogenic habitat loss and fragmentation worm species (strongyle type, including Murshidia,
(Ambu et al. 2012). Asian elephants, including Bor- Quilonia, Bathmostomum, Grammocephalus and
nean elephants, are listed by the IUCN as Endangered Equinurbia). These parasites in Asian elephants may
(Choudhury et al. 2008). Bornean elephants are mor- be associated with pathology, clinical disease, in-
phometrically distinct, with larger ears, longer tails, creased morbidity and mortality. Gastrointestinal
straighter tusks and a more rounded body shape than nematode infection is associated with frequent clini-
Asian elephants on the mainland (Othman et al. cal illness, including colic, diarrhoea and dependent
2008). Arguably, Bornean elephants are a genetically oedema in Asian elephants managed in captivity in
distinct subspecies of Asian elephant and constitute Kerala, India (Saseendran et al. 2004, Chandra-
an evolutionary significant conservation unit (Fer- sekharan et al. 2009), and in Asian elephants in the
nando et al. 2003). Regardless of their origins, Bor- Myanmar timber industry, gastrointestinal round-
nean elephants are a conservation priority as an worms and liver flukes directly account for 8% of
iconic flagship and umbrella species carrying out vital deaths (n = 2806) and contribute to 13% of deaths
ecosystem services (Campos-Arceiz & Corlett 2011). associated with ‘weakness’ (Mar 2007).
An estimated 2040 (95% CI: 1184−3652) Bornean ele- Neglect of parasite research in conservation and the
phants remain confined to 4 managed ranges, includ- practical challenges of field parasitology have pre-
ing the 2 study sites of the present study: the Lower cluded surveys of wild Asian elephants in range coun-
Kinabatangan Wildlife Sanctuary (LKWS) and the tries. This study addresses the absence of baseline
Tabin Wildlife Reserve (TWR) (Alfred et al. 2010). data on parasites of endangered species and is the first
No previously reported studies have included par- parasite survey in endangered Bornean elephants.
asites of endangered Bornean elephants, captive or
wild. Indeed, surveys to assess parasite prevalence
and load in Asian elephants are seldom reported in MATERIALS AND METHODS
the literature. Collating data largely from captive
Asian elephants, Fowler & Mikota (2006) catalogued Study sites
parasites including: trematodes or liver flukes (Fasci-
ola spp.), cestodes or tapeworms (Anoplocephala The LKWS (5° 18’ N to 5° 42’ N, 117° 54’ E to 118°
spp.) and various gastrointestinal nematode or round- 33’ E is a highly fragmented mosaic of forest patches
 Hing et al.: Bornean elephant endoparasites 225

in an agricultural-dominated landscape with signifi- burn & Butler 2006), supernatant was removed and
cant ongoing anthropogenic impact including vil- the wet weight was recorded.
lages, small-scale agriculture, oil palm plantations
and a busy tourism industry. The LKWS is home to an
estimated 298 elephants (95% CI: 152−581) at a den- Sample analysis
sity of 2.15 Bornean elephants per km2 (Alfred et al.
2010). The population density of Bornean elephant in Samples were analysed following published proto-
the LKWS is very high, when it is considered that the cols for the special modification of the McMaster
minimum viable area for Asian elephants is 0.5 to 1.5 method of faecal egg flotation to a sensitivity of
elephants per km2 (Sukumar 2003). 10 ova g–1 faeces (MAFF 1986). Parasite ova were ob-
The TWR (5° 10 N to 5° 15 N, 118° 30’ E to 118° 45’ E, served using an Omax digital binocular compound
the largest continuous in Sabah with an area of ap- light microscope (Model MD827S30 series) and
proximately 1200 km2, consists of secondary diptero- photographs were captured with the microscopic
carp forest and scattered pockets of remnant primary imaging software ScopeImage 9.0 H3D. Ova were
forest. The TWR has a total population of 342 Bornean identified to phylum level based on morphology and
elephants (95% CI: 152−774) at a density of 0.6 indi- morphometrics.
viduals per km2 (Alfred et al. 2010). Prevalence, the number of positive cases as a per-
centage of the total number sampled, was calculated
as an indication of how common parasite infection
Sample collection was in each population. Faecal egg count (FEC), an
indirect measure of the parasite load of an individual
During the dry season, 104 faecal samples were col- host, was calculated in terms of eggs g–1 faeces (EPG).
lected from free-ranging wild Bornean elephants in A diversity score of 1, 2 or 3 was assigned according to
the LKWS (n = 52) and the TWR (n = 52) (Fig. 2). The the number of parasite types observed in each
approximate location of wild Bornean elephants was sample, where 3 indicates the presence of ova of Fas-
ascertained using data from satellite collars and re- ciola, Anoplocephala and strongyle-type species.
ports from local contacts. Animals were tracked on
foot using VHF radio tracking and indirect signs
including footprints, dung piles and evidence of feed- Statistical analysis
ing on vegetation. The latitude and longitude of sam-
ple collection sites were recorded using a handheld Prevalence, load and diversity of parasites were
GPS (Garmin GPS MAP 60CSx). compared between samples from the LKWS and the
Freshly deposited faeces were identified for col- TWR. Using R 2.14.1, a chi-squared test was applied to
lection by appearance (colour, consistency and ob- compare parasite prevalence between sites and a Wil-
served insect activity). Core samples
were collected from faecal boluses of Protected
areas
different sizes to reduce contamina- Sample
tion by soil nematodes. Several collection
locations
boluses in a dung pile were sampled Rivers
to ensure that the resulting pooled
sample was representative. To min-
imise duplication, i.e. the inadvertent
repeated collection of faecal samples
LKWS
from the same individuals, elephants
were observed and boluses of differ- TWR
ent sizes were sampled from dung
piles located at a distance of at least Sabah,
Malaysia
5 m from one another. Samples were
collected in labelled, pre-prepared
polyethylene specimen containers
containing 95% ethanol. Ethanol- Fig. 2. Sample collection locations in the Lower Kinabatangan Wildlife Sanctu-
fixed faecal samples were centrifuged ary (LKWS) and the Tabin Wildlife Reserve (TWR). Inset shows the study
to maximise parasite detection (Blag- location in Sabah, Malaysia
226 Endang Species Res 21: 223–230, 2013

coxon Mann-Whitney U-test was employed to com- TWR compared with the LKWS (χ2 = 10.34, df = 102,
pare parasite load and diversity between sites. Using p < 0.05). Conversely, the prevalence of strongyles
Microsoft Excel 2010, a variance to mean ratio (VAR), (χ2 = 4.98, df = 102, p < 0.05) and Anoplocephala (χ2 =
also known as a coefficient of dispersion, was calcu- 15.38, df = 102, p < 0.05) were significantly higher in
lated to assess the distribution of parasite load data. the LKWS compared with the TWR (Table 1).

RESULTS Parasite load

Endoparasites were found to be ubiquitous in The load of each parasite type was significantly dif-
Bornean elephants, with all samples yielding at least ferent between sites. The mean load of Fasciola was
one parasite ovum. Parasite phyla detected included significantly higher in the TWR (238.0 EPG) than in
trematodes, cestodes and nematodes. Trematodes the LKWS (86.2 EPG; Mann-Whitney test statistic
were represented by Fasciola species (Fig. 3A), ces- W = 858.5, p < 0.05). Conversely, the mean load of
todes by Anoplocephala species (Fig. 3B) and nema- strongyles was significantly higher in the LKWS
todes by strongyle-type ova (Fig. 3C). Due to over- (155.4 EPG) than in the TWR (81.3 EPG; W = 1873,
lapping size of strongyle ova produced by different p < 0.05). The mean load of Anoplocephala was also
parasites, they could not be reliably identified to significantly higher in the LKWS (101.8 EPG) com-
genus or species level. pared with the TWR (37.6 EPG; W = 1928.5, p < 0.05;
Table 2). For each parasite type in each location and
parasite load data overall, VAR was >1, which is
Prevalence indicative of overdispersion.

Fasciola (liver fluke) was found to be the most

prevalent endoparasite overall, with 70.2% (73 posi- Mixed infection
tive cases/104 total samples) of elephants infected.
Strongyle (66.3%, 69/104) and Anoplocephala The majority of samples (65.4%, 68/104) yielded
(50.0%, 52/104) infections were also frequently iden- more than one phylum of endoparasite, but mixed
tified (Table 1).
In the LKWS, strongyle nematodes (82.7%, 43/52)
Table 1. Prevalence of parasitic ova in the Lower Kinaba-
were the most prevalent endoparasites; Anoploce- tangan Wildlife Sanctuary (LKWS) and the Tabin Wildlife
phala (69.2%, 36/52) and Fasciola (55.7%, 29/52) Reserve (TWR). Values in parentheses are the number of
were also widespread. In the TWR, Fasciola (84.6%, positive cases/the total number sampled
44/52) was the most prevalent endoparasite. Stron-
gyles (50.0%, 26/52) and Anoplocephala (30.8%, Parasite type Positive samples (%)
16/52) were also common (Table 1). LKWS TWR Total
A preliminary comparison between the prevalence
Fasciola 55.7 (29/52) 84.6 (44/52) 70.2 (73/104)
of trematodes, cestodes and nematodes in the LKWS
Anoplocephala 69.2 (36/52) 30.8 (16/52) 50.0 (52/104)
and the TWR revealed significant differences. The Strongyles 82.7 (43/52) 50.0 (26/52) 66.2 (69/104)
prevalence of Fasciola was significantly higher in the

Fig. 3. Parasite ova identified in Elphas maximum borneenis. (A) Fasciola ovum; (B) Anoplocephala ovum; (C) strongyle-type
ovum. Green lines show length (L)
 Hing et al.: Bornean elephant endoparasites 227

infections were more prevalent in the TWR (80.8%, genic activities, and this warrants further investiga-
42/52) compared with the LKWS (50.0%, 26/52; tion as part of the conservation management of
χ2 = 10.83, df = 1, p < 0.05; Table 3). Bornean elephants and their habitat.
The prevalence and load of each phylum will be
discussed separately, as different types of parasites
DISCUSSION have different life cycles and routes of transmission
and thus are affected by different host, parasite and
This study provides the first baseline data on endo- environmental factors.
parasites in wild Bornean elephants. All wild animals The results of this study agree with previous stud-
harbour parasites of some kind because hosts and ies on trematodes in Asian elephants which indicate
parasites have coevolved over millennia, developing that Fasciola species are prevalent and present in
complex systems which can vary from commensal to high numbers. Trematodes are amongst the most fre-
highly virulent (Anderson & May 1982, Toft & Karter quently encountered endoparasites in captive Suma-
1990, Taylor et al. 2013). While it is expected that tran elephants (Stremme et al. 2007), and 33.8% of
Bornean elephants harbour parasites, the findings of semi-captive Asian elephants surveyed in Nepal are
this study have potential long-term health and con- infected with Fasciola (Karki 2008).
servation implications. Firstly, the high prevalence The high overall prevalence of Fasciola found in
and load of strongyles and Anoplocephala in the Bornean elephants may be associated with the wet
LKWS and Fasciola in the TWR may have clinical sig- tropical conditions in Sabah, which are ideal for the
nificance, particularly if compounded by concurrent complex, freshwater-dependent life cycle of Fasciola
disease and other factors such as stress. The results species. Fasciola ova hatch and release miracidia,
also indicate a high potential for transmission of dis- which enter aquatic lymnaeid snails, develop through
eases spread via similar routes to the parasites iden- several life stages in these intermediate hosts and
tified. In addition, significant differences in parasite eventually emerge from the snails as cercariae,
prevalence and load between fragmented and con- which encyst on aquatic plants. Cercariae mature
tinuous habitat may be associated with anthropo- into metacercariae (infective stage) and definitive
hosts become infected by ingesting vegetation or
water harbouring metacercariae (Taylor et al. 2013).
Table 2. Parasite load (avg. no. of ova g–1 faeces) in the
Metacercariae can persist for up to 8 mo in moist con-
Lower Kinabatangan Wildlife Sanctuary (LKWS) and the
Tabin Wildlife Reserve (TWR) ditions and fodder such as that upon which wild
Bornean elephants feed (Fowler & Mikota 2006).
There are several possible factors which may con-
Parasite type LKWS TWR Mean load across
both sites tribute to the observed higher Fasciola prevalence
and load in the TWR compared with the LKWS. Inter-
Fasciola 86.2 238.0 162.1 mediate hosts for Fasciola, aquatic lymnaeid snails,
Anoplocephala 101.8 37.6 69.7
may be more abundant in the TWR compared with
Strongyles 155.4 81.3 118.4
Total mean load 343.4 356.9 350.2 the LKWS, increasing the probability that infectious
metacercariae are present in the TWR. Water bodies
in some parts of the TWR are further away from palm
Table 3. Mixed infections in the Lower Kinabatangan oil plantations than water bodies in the LKWS.
Wildlife Sanctuary (LKWS) and the Tabin Wildlife Reserve
Therefore, water bodies in the LKWS may contain
(TWR). A diversity score of 1, 2 or 3 was assigned according
to the number of parasite types observed in each sample, greater levels of agricultural pollutants such as palm
where 3 indicates the presence of ova of Fasciola, Anoplo- oil mill effluent than those in the TWR. Palm oil mill
cephala and strongyle-type species. Values in parentheses effluent is generally pH 4 to 5 due to organic acids
are the number of samples scoring a diversity score of 1, 2 produced in the fermentation process (Ma 1999,
or 3/the total number sampled
Lorestani 2006), but lymnaeid snails prefer near-neu-
tral pH (Laursen et al. 1989). Alternatively, Bornean
Site Frequency of parasite diversity scores (%)
1 2 3 elephants in the TWR may feed on aquatic vegeta-
tion more frequently than those in the LKWS, as
LKWS 50.0 (26/52) 34.6 (18/52) 15.4 (8/52) anthropogenic activities often impede access to the
TWR 19.2 (10/52) 48.1 (25/52) 32.7 (17/52) banks of the Kinabatangan River.
Total across 34.6 (36/104) 41.3 (43/104) 24.0 (25/104)
Factors influencing prevalence and load may vary
both sites
depending on the species of Fasciola. Although ova
228 Endang Species Res 21: 223–230, 2013

could not be identified to species level in this study, parasite infection (Dhabhar & McEwen 1997, Agar-
they were likely to be either F. hepatica and/or F. wal & Marshall 2001). Nutritional stress such as lim-
jacksoni (Fowler & Mikota 2006, Karki 2008). Fasciola ited food availability and deficiencies in dietary com-
jacksoni is an Asian-elephant-specific fasciolid, where- ponents, particularly protein and energy, influence
as a variety of mammals play host to F. hepatica; thus susceptibility to parasites and pathogens (Chapman
prevalence and load are affected by a suite of other et al. 2006b). Dietary stress and parasitism in African
epidemiological factors, such as density of livestock in elephants Loxodonta africana in Kenya have a syner-
surrounding areas (Ai et al. 2011). Further research, gistic effect, leading to mass mortalities (Obanda
including species differentiation, observations of Bor- 2011). Bornean elephants in the fragmented habitat
nean elephant feeding behaviour, water quality as- of the LKWS may also experience stress associated
sessments and lymnaeid snail surveys, are warranted. with frequent and intense anthropogenic activities,
The prevalence of trematodes correlates positively though further research is required to confirm this
with the abundance of definitive wildlife hosts of var- assumption. Further studies to investigate physiolog-
ious taxa (Fredensborg et al. 2006, Byers et al. 2011). ical parameters, particularly faecal glucocorticoid
Following this pattern, significant differences in pre- metabolites, are warranted.
valence of Fasciola in the TWR compared with the The frequency of mixed infections suggests that
LKWS may reflect a greater total number of Bornean Bornean elephants are susceptible to a myriad of par-
elephants at the former site (Alfred et al. 2010). asites and that environmental conditions in Sabah
A high prevalence and load of Anoplocephala in are conducive to parasite survival and transmission.
other herbivores is associated with sustained grazing These conditions make parasitological research all
of permanent pasture and microenvironmental con- the more relevant for the conservation of wildlife and
ditions favourable to oribatid mites, the intermediate their symbiotic fauna in Borneo, a global biodiversity
hosts of Anoplocephala (Ihler et al. 1995, McAloon hotspot (Gómez et al. 2012). A higher frequency of
2004). In the LKWS, habitat fragmentation precludes mixed infections in the continuous forest of the TWR
Bornean elephant movement to new feeding grounds. compared with the fragmented habitat of the LKWS
Consequently, the sustained use of existing feeding may be a reflection of overall biodiversity in continu-
grounds by Bornean elephants in the LKWS over ous versus fragmented habitat. Continuous habitat
numerous consecutive years is likely to increase the harbours greater species diversity than smaller, more
prevalence and load of Anoplocephala as well as disconnected patches, and this concept may also
strongyle nematodes. apply to parasites (MacArthur & Wilson 1967, Robin-
Strongyles are inadvertently ingested by their son & Quinn 1992, Fahrig 2003, Nunn et al. 2003).
hosts as infective third-stage larvae on vegetation. Parasite overdispersion, the variable distribution of
The overall high prevalence and load of strongyle parasites in any given animal population whereby
nematodes indicates a high potential for faecal−oral the majority of parasites is found in a small fraction of
transmission of parasites and pathogens in Bornean the host population, is a central paradigm in parasite
elephants. The high prevalence of strongyles is par- ecology because factors that produce overdisperson
ticularly concerning as parasites whose transmission are key to understanding host parasite co-evolution,
is facilitated by close contact have been shown to be infection dynamics and disease risk (Wilson et al.
more likely to increase the risk of extinction com- 2003). Mortality and morbidity associated with para-
pared with those transmitted by other routes (Peder- sites is typically dose-dependent and therefore has
sen et al. 2007). the greatest impact on the small fraction of hosts that
The higher population density of Bornean ele- harbour the majority of parasites (Wilson et al. 2003).
phants in the LKWS compared with the TWR is a VAR >1 indicates an overdispersion of parasites in
plausible explanation for the significantly higher endangered Bornean elephants, which may be deter-
prevalence and load of strongyles in the former pop- mined by heterogeneity of gender, age, body condi-
ulation. High population density facilitates faecal− tion, exposure, genetics, immunity, feeding behav-
oral transmission and is a key factor contributing to iour and habitat characteristics (Wassom et al. 1986).
prevalence, load and diversity of nematodes (Wierg- Further research is warranted to improve our under-
ertjes & Flik 2004, Lebarbenchon et al. 2006). standing of how these factors affect parasite overdis-
Alternative explanations for the higher strongyle persion and, consequently, host survival. In particu-
prevalence in the LKWS compared with the TWR lar, overdispersion of strongyle nematodes in the
include physiological and nutritional stress. Stress densely populated LKWS demands attention be-
affects host immunity and predisposes animals to cause it has been shown that overdispersion is a key
 Hing et al.: Bornean elephant endoparasites 229

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sity affects infection dynamics (Churcher et al. 2005) Alfred R (2012) Asian elephant action plan. Sabah Wildlife
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Editorial responsibility: Nils Bunnefeld, Submitted: February 11, 2013; Accepted: July 2, 2013
Stirling, UK Proofs received from author(s): August 30, 2013