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Exposure of Wild Sumatran Tiger (Panthera tigris sumatrae) to Canine Distemper Virus

Authors:
Mulia Huaso Bongot at Taman Safari Indonesia
Mulia Huaso Bongot
  • Taman Safari Indonesia
Silmi Mariya
Silmi Mariya
Silmi Mariya
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Jessica Bodgener at University of Kent
Jessica Bodgener
Diah Iskandriati at IPB University
Diah Iskandriati
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Abstract

Canine distemper virus (CDV) is recognized as a conservation threat to Amur tigers (Panthera tigris altaica) in Russia, but the risk to other subspecies remains unknown. We detected CDV neutralizing antibodies in nine of 21 wild- caught Sumatran tigers (42.9%), including one sampled on the day of capture, confirming exposure in the wild.
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Exposure of Wild Sumatran Tiger (Panthera tigris
sumatrae) to Canine Distemper Virus
Authors: Mulia, Bongot Huaso, Mariya, Silmi, Bodgener, Jessica,
Iskandriati, Diah, Liwa, Setyaningsih Rambu, et al.
Source: Journal of Wildlife Diseases, 57(2) : 464-466
Published By: Wildlife Disease Association
URL: https://doi.org/10.7589/JWD-D-20-00144
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DOI: 10.7589/JWD-D-20-00144 Journal of Wildlife Diseases, 57(2), 2021, pp. 464–466
ÓWildlife Disease Association 2021
Exposure of Wild Sumatran Tiger (Panthera tigris sumatrae) to Canine
Distemper Virus
Bongot Huaso Mulia,
1
Silmi Mariya,
2
Jessica Bodgener,
3
Diah Iskandriati,
2
Setyaningsih Rambu Liwa,
1
Tony Sumampau,
1
Jansen Manansang,
1
Huda S. Darusman,
2
Steven A. Osofsky,
3
Navapon
Techakriengkrai,
4,5,6
and Martin Gilbert
3,6
1
Taman Safari Indonesia, Jalan Kapten Harun Kabir No. 724,
Cibeureum, Cisarua, Bogor, 16750, Indonesia;
2
Primate Research Center, Institute of Research and Community Service,
Bogor Agricultural University (IPB University), Jalan Lodaya ll/5, Bogor, 16151, Indonesia;
3
Cornell Wildlife Health Center,
Wild Carnivore Health Program, College of Veterinary Medicine, Cornell University, 240 Farrier Road, Ithaca, New York
14853, USA;
4
Department of Veterinary Microbiology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok,
10330, Thailand;
5
Diagnosis and Monitoring of Animal Pathogens Research Unit, Chulalongkorn University, Bangkok,
10330, Thailand;
6
Corresponding authors (emails: Navapon.T@chula.ac.th; m.gilbert@cornell.edu)
ABSTRACT: Canine distemper virus (CDV) is
recognized as a conservation threat to Amur tigers
(Panthera tigris altaica) in Russia, but the risk to
other subspecies remains unknown. We detected
CDV neutralizing antibodies in nine of 21 wild-
caught Sumatran tigers (42.9%), including one
sampled on the day of capture, confirming
exposure in the wild.
As populations of threatened species such
as tigers (Panthera tigris) continue to decline
and fragment, they become increasingly
vulnerable to stochastic events such as infec-
tious disease outbreaks. Since 2003, infection
with canine distemper virus (CDV) has been
responsible for mortality of endangered Amur
tigers (P. tigris altaica) in Russia and is
estimated to increase the 50-yr extinction
probability of small populations of 25 individ-
uals by as much as 65% (Seimon et al. 2013;
Gilbert et al. 2014, 2015, 2020). There is an
urgent need to evaluate the CDV infection
status of other tiger subspecies, to determine
the potential threat to these vulnerable
populations. Testing strategies based on the
detection of pathogens (such as reverse
transcriptase-PCR) are more useful for syn-
dromic surveillance, where infection is sug-
gested by clinical presentation for agents such
as CDV that are associated with acute disease
and short periods of shedding. These ap-
proaches can lead to epidemiologically valu-
able information (such as sequence data) but
are limited by the infrequency of sampling
opportunities for what are liable to be rare
infection events in a species that is seldom
handled. Serological approaches can repre-
sent a more cost-effective strategy to detect
population exposure to pathogens such as
CDV that evoke a strong and long-lasting
humoral immune response in animals that
recover from infection (Greene and Appel
2006; Brown et al. 2010). We sought to
determine whether wild populations of Suma-
tran tigers (P. tigris sumatrae) have been
exposed to CDV, as a first step toward
determining the potential threat that the virus
might represent to the subspecies.
Sumatran tigers are classified as critically
endangered by the International Union for the
Conservation of Nature, with fewer than 500
individuals thought to exist in the wild (Linkie
et al. 2008). Remaining habitat is highly
fragmented and, although tiger sign has been
positively identified in 33 areas (Wibisono and
Pusparini 2010), many populations are small,
isolated, and vulnerable to stochastic process-
es such as infectious disease introductions.
Serum samples were collected from 21
Sumatran tigers captured from the wild
between 1988 and 2016. All captures were
carried out as part of routine wildlife man-
agement and conflict resolution, with the
exception of three tigers injured by snares.
All 21 tigers were transferred to the zoological
collection Taman Safari Indonesia (Bogor,
West Java), where samples were collected by
park veterinarians. These samples were then
stored at 80 C and heat inactivated at 56 C
for 30 min prior to testing. Serum neutraliza-
tion assays were conducted as described by
Logan et al. (2016), using HEK293 cells
expressing canine signaling lymphocytic acti-
vation molecule (SLAM-F1, the receptor used
by CDV for cell entry) and a replication-
464
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deficient vesicular stomatitis virus pseudotype
expressing hemagglutinin and fusion surface
glycoproteins from the Onderstepoort strain
of CDV. The referenced protocol was adapted
slightly by substituting green fluorescent
protein for luciferase to indicate infection,
which negated the need for a luminometer.
All assays were run in quadruplicate using
four-fold serial serum dilutions ranging from
1:16 to 1:16,384. Fluorescent cells were
counted manually in each well, with antibody
titers determined as the highest dilution with
90% reduction in infected cells compared to
the average count from four serum-free
control wells. Final titers were calculated
using the Spearman-Karber method (Lorenz
and B¨
ogel 1973), and a titer of 1:16 or higher
was considered positive.
A total of nine samples were positive (42.9%,
95% confidence interval: 21.8–66.0%, n¼21)
with titers ranging from 1:128 to .1:16,384. Of
these, eight positive samples were collected
between 6 mo and 20 yr after capture from the
wild, preventing differentiation of wild expo-
sures from infections possibly contracted while
in captivity. None of the tigers showed clinical
signs indicative of CDV infection on the day of
capture. The longevity of circulating antibodies
in tigers that have recovered from CDV
infection is unknown, but in dogs, neutralizing
antibodies remain detectable for many years
and possibly the remainder of the animal’slife
(Bohm et al. 2004; Greene and Appel 2006).
Although no cases of clinical disease consistent
with CDV had been recorded in the facility
where these eight positive tigers were held, all
were housed in enclosures with the potential
for access by wild civets or other susceptible
wildlife, representing a possible route for
captive infection. One adult male tiger that
was rescued from a snare in Bengkulu
province, was found to have a titer of 1:8,192
and had been sampled by Taman Safari
Indonesia veterinarians on the day of capture
(12 January 2012), providing clear evidence
that exposure had occurred in the wild. This
tiger subsequently died from his injuries,
apparently unrelated to CDV. The eight other
seropositive tigers originated from Aceh, North
Sumatra, and Bengkulu provinces.
Our pilot study confirms the occurrence of
infection, but is unable to assess extent of
exposure, which would be critical to evaluate
the threat that CDV represents for Sumatran
tiger populations. This could be rectified by
routinely analyzing serum samples collected
whenever wild tigers are captured for conflict
resolution, rehabilitation, or biological re-
search. In Russia since 2000, CDV seroprev-
alence in Amur tiger populations has been
measured as 37.0% (confidence interval: 24.6–
51.3%, n¼54, Gilbert et al. 2020), providing a
source of comparison. Furthermore, field staff
and wildlife managers should be familiarized
with the clinical profile of CDV in tigers,
principally neurological disease (unusual be-
havior, loss of fear, loss of aggression,
blindness, ataxia, and/or seizures), and possi-
bly respiratory and gastrointestinal signs. In
these cases, diagnostic testing (reverse tran-
scription polymerase chain reaction with
sequencing confirmation) of antemortem sam-
ples (whole blood, serum, conjunctival swabs,
and/or urine), and postmortem samples (in-
cluding brain tissue, lymph nodes, lung, and
bladder) should become routine (see Seimon
et al. 2013 for protocols). Demonstration of
supporting histopathology and possibly use of
immunohistochemistry would also be valu-
able. Widespread exposure would indicate the
need to develop population viability models
integrating CDV epidemiology to explore the
impact of infection scenarios and identify
populations at particular risk. Where re-
quired, epidemiological research aimed at
identifying CDV reservoirs for Sumatran
tigers would be essential to inform appropri-
ate mitigation strategies, including the poten-
tial for vaccination of reservoir species or
tigers themselves.
We would like to thank the Directorate of
Biodiversity Conservation (Konservasi Keane-
karagaman Hayati) in Indonesia for endorsing
this work, and the Cornell Feline Health
Center and Cornell Wildlife Health Center
for financial support. N.T. received a Schol-
arship for Research Abroad, Kanchanaphisek
Chalermprakiet Endowment Fund from the
Office of International Affairs and Global
Network, Chulalongkorn University, and the
LETTERS 465
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Thailand Research Fund (TRF Senior Schol-
ar, RTA6080012).
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466 JOURNAL OF WILDLIFE DISEASES, VOL. 57, NO. 2, APRIL 2021
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... pardus orientalis) in the Russian Far East [15,16,27,33]. Elsewhere, CDV infections have been confirmed in free-ranging tigers and leopards in Indonesia and India [12][13][14]. Most cases presented with neurological signs including disorientation and a lack of fear. ...
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Full-text available
  • Sep 2022
Simple Summary Canine distemper virus (CDV) is the etiological agent of a highly frequent viral disease of domestic and wild carnivores. It poses a threat for the conservation of endangered species. Our aim was to assess the presence and phylogenetic characterization of CDV from naturally infected Crab-eating Fox (Cerdocyon thous) from Colombia. We confirm for the first time the circulation of CDV South America/North America-4 Lineage in Crab-eating Fox. Our results are crucial for the understanding of the interspecies transmission of CDV in the domestic/wild interface and for the prevention and control of such an important multi-host pathogen. Abstract Canine distemper virus (CDV) is the etiological agent of a highly prevalent viral infectious disease of domestic and wild carnivores. This virus poses a conservation threat to endangered species worldwide due to its ability to jump between multiple species and produce a disease, which is most often fatal. Although CDV infection has been regularly diagnosed in Colombian wildlife, to date the molecular identity of circulating CDV lineages is currently unknown. Our aim was to evaluate the presence and phylogenetic characterization of CDV detected in samples from naturally infected Cerdocyon thous from Colombia. We sequenced for the first time the CDV infecting wildlife in Colombia and demonstrated the presence of South America/North America-4 Lineage with a higher relationship to sequences previously reported from domestic and wild fauna belonging to the United States of America. Our results are crucial for the understanding of the interspecies transmission of CDV in the domestic/wild interface and for the prevention and control of such an important multi-host pathogen.
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Snaring in a stronghold: Poaching and bycatch of critically endangered tigers in northern Sumatra, Indonesia
Article
Full-text available
  • Oct 2023
  • BIOL CONSERV
Wire-snare poaching is increasingly recognized as a major threat to endangered large carnivores in Africa and Asia. However, empirical information on the extent and distribution of snaring remains extremely limited beyond anecdotal reports presenting opportunistically collected data. In this study, we compile information to present a comprehensive synopsis of snaring of critically endangered Sumatran tigers (Panthera tigris sumatrae). Hunted for their parts and skins, Sumatran tigers remain in high demand in illicit international markets. We focus our analysis on the provinces of Aceh and North Sumatra, Indonesia, which cumulatively contain ~36 % of the island’s remaining tiger habitat. Based on records collected from a combination of Indonesian government data, ranger patrol observations, and content analysis of local media, we identified 13 tiger snaring hotspots and documented 28 verified incidents of ensnared tigers between March 2008–March 2023. These totals represent minimum estimates because of spatiotemporal gaps in ranger patrols and inconsistent reporting of snaring by local communities. Our analysis of the incidents reveals tiger mortality in 9 (32.1 %) of the cases and permanent moves to ex-situ settings due to amputation or other debilitating snaring-induced injuries in another 8 (28.6 %) cases. Tiger snaring was positively correlated with forest-edge habitats in the Leuser Ecosystem, where 64.3 % of all incidents occurred. Across both provinces, 28.6 % of all snared tigers were allegedly captured in snares set in agricultural areas to control wild boar. To maximize efficacy of the government’s ongoing anti-snare campaigns, we recommend increased personnel for ranger patrols and more attention on tiger-specific snaring impacts.
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Distemper, extinction, and vaccination of the Amur tiger
Article
Full-text available
  • Nov 2020
Significance The decline and progressive fragmentation of many threatened populations increase extinction vulnerability due to outbreaks of infectious disease. Vaccination is one of the few tools available to mitigate these threats, but its use is often hampered by insufficient epidemiological understanding and historic controversies over endangered wildlife vaccination. Using the example of Amur tigers and CDV, we describe a holistic approach to select appropriate disease mitigation strategies based on key epidemiological evidence from the field. We then assess the protection of vaccinated tigers against the locally circulating CDV strain and use modeling to compare the efficacy and cost of potential vaccination programs. This practical approach provides conservation managers with an evidence-based rationale to address disease-mediated extinction risks for threatened wildlife populations.
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Efficient generation of vesicular stomatitis virus (VSV)-pseudotypes bearing morbilliviral glycoproteins and their use in quantifying virus neutralising antibodies
Article
Full-text available
  • Dec 2015
Morbillivirus neutralising antibodies are traditionally measured using either plaque reduction neutralisation tests (PRNTs) or live virus microneutralisation tests (micro-NTs). While both test formats provide a reliable assessment of the strength and specificity of the humoral response, they are restricted by the limited number of viral strains that can be studied and often present significant biological safety concerns to the operator. In this study, we describe the adaptation of a replication-defective vesicular stomatitis virus (VSVΔG) based pseudotyping system for the measurement of morbillivirus neutralising antibodies. By expressing the haemagglutinin (H) and fusion (F) proteins of canine distemper virus (CDV) on VSVΔG pseudotypes bearing a luciferase marker gene, neutralising antibody titres could be measured rapidly and with high sensitivity. Further, by exchanging the glycoprotein expression construct, responses against distinct viral strains or species may be measured. Using this technique, we demonstrate cross neutralisation between CDV and peste des petits ruminants virus (PPRV). As an example of the value of the technique, we demonstrate that UK dogs vary in the breadth of immunity induced by CDV vaccination; in some dogs the neutralising response is CDV-specific while, in others, the neutralising response extends to the ruminant morbillivirus PPRV. This technique will facilitate a comprehensive comparison of cross-neutralisation to be conducted across the morbilliviruses.
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Canine distemper virus as a threat to wild tigers in Russia and across their range
Article
Full-text available
  • May 2015
  • Integr Zool
Canine distemper virus (CDV) has recently been identified in populations of wild tigers in Russia and India. Tiger populations are generally too small to maintain CDV for long periods, but are at risk of infections arising from more abundant susceptible hosts that constitute a reservoir of infection. Because CDV is an additive mortality factor, it could represent a significant threat to small, isolated tiger populations. In Russia, CDV was associated with the deaths of tigers in 2004 and in 2010, and was coincident with a localized decline of tigers in Sikhote-Alin Zapovednik, (from 25 tigers in 2008 to nine in 2012). Habitat continuity with surrounding areas likely played an important role in promoting an on-going recovery. We recommend steps be taken to assess the presence and the impact of CDV in all tiger range states, but should not detract focus away from the primary threats to tigers, which include habitat loss and fragmentation, poaching and retaliatory killing. Research priorities include: 1) recognition and diagnosis of clinical cases of CDV in tigers when they occur, and 2) collection of baseline data on the health of wild tigers. CDV infection of individual tigers need not imply a conservation threat, and modeling should complement disease surveillance and targeted research to assess the potential impact to tiger populations across the range of ecosystems, population densities and climate extremes occupied by tigers. Describing the role of domestic and wild carnivores as contributors to a local CDV reservoir is an important precursor to considering control measures.This article is protected by copyright. All rights reserved
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Estimating the Potential Impact of Canine Distemper Virus on the Amur Tiger Population (Panthera tigris altaica) in Russia
Article
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Lethal infections with canine distemper virus (CDV) have recently been diagnosed in Amur tigers (Panthera tigris altaica), but long-term implications for the population are unknown. This study evaluates the potential impact of CDV on a key tiger population in Sikhote-Alin Biosphere Zapovednik (SABZ), and assesses how CDV might influence the extinction potential of other tiger populations of varying sizes. An individual-based stochastic, SIRD (susceptible-infected-recovered/dead) model was used to simulate infection through predation of infected domestic dogs, and/or wild carnivores, and direct tiger-to-tiger transmission. CDV prevalence and effective contact based on published and observed data was used to define plausible low- and high-risk infection scenarios. CDV infection increased the 50-year extinction probability of tigers in SABZ by 6.3% to 55.8% compared to a control population, depending on risk scenario. The most significant factors influencing model outcome were virus prevalence in the reservoir population(s) and its effective contact rate with tigers. Adjustment of the mortality rate had a proportional impact, while inclusion of epizootic infection waves had negligible additional impact. Small populations were found to be disproportionately vulnerable to extinction through CDV infection. The 50-year extinction risk in populations consisting of 25 individuals was 1.65 times greater when CDV was present than that of control populations. The effects of density dependence do not protect an endangered population from the impacts of a multi-host pathogen, such as CDV, where they coexist with an abundant reservoir presenting a persistent threat. Awareness of CDV is a critical component of a successful tiger conservation management policy.
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Canine Distemper Virus: an Emerging Disease in Wild Endangered Amur Tigers (Panthera tigris altaica)
Article
Full-text available
  • Aug 2013
Unlabelled: Fewer than 500 Amur tigers (Panthera tigris altaica) remain in the wild. Due to low numbers and their solitary and reclusive nature, tiger sightings across their range in the Russian Far East and China are rare; sightings of sick tigers are rarer still. Serious neurologic disease observed in several wild tigers since 2001 suggested disease emergence in this endangered species. To investigate this possibility, histology, immunohistochemistry (IHC), in situ hybridization (ISH), and reverse transcription-PCR (RT-PCR) were performed on tissues from 5 affected tigers that died or were destroyed in 2001, 2004, or 2010. Our results reveal canine distemper virus (CDV) infection as the cause of neurologic disease in two tigers and definitively establish infection in a third. Nonsuppurative encephalitis with demyelination, eosinophilic nuclear viral inclusions, and positive immunolabeling for CDV by IHC and ISH were present in the two tigers with available brain tissue. CDV phosphoprotein (P) and hemagglutinin (H) gene products were obtained from brains of these two tigers by RT-PCR, and a short fragment of CDV P gene sequence was detected in lymph node tissue of a third tiger. Phylogenetically, Amur tiger CDV groups with an Arctic-like strain in Baikal seals (Phoca siberica). Our results, which include mapping the location of positive tigers and recognition of a cluster of cases in 2010, coupled with a lack of reported CDV antibodies in Amur tigers prior to 2000 suggest wide geographic distribution of CDV across the tiger range and recent emergence of CDV as a significant infectious disease threat to endangered Amur tigers in the Russian Far East. Importance: Recognition of disease emergence in wildlife is a rare occurrence. Here, for the first time, we identify and characterize a canine distemper virus (CDV), the second most common cause of infectious disease death in domestic dogs and a viral disease of global importance in common and endangered carnivores, as the etiology of neurologic disease and fatal encephalitis in wild, endangered Amur tigers. We establish that in 2010 CDV directly or indirectly killed -1% of Amur tigers. Location of positive cases over an expansive geographic area suggests that CDV is widely distributed across the tiger range. Interspecies interactions are increasing as human populations grow and expand into wildlife habitats. Identifying animal reservoirs for CDV and identifying the CDV strains that are transmissible to and among wildlife species, including Amur tigers and sympatric critically endangered Amur leopards (Panthera pardus orientalis), is essential for guiding conservation and mitigation efforts.
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Sumatran tiger (Panthera tigris sumatrae): A review of conservation status
Article
Full-text available
  • Dec 2010
  • Integr Zool
The majority of wild Sumatran tigers are believed to live in 12 Tiger Conservation Landscapes covering approximately 88,000 km(2) . However, the actual distribution of tigers across Sumatra has never been accurately mapped. Over the past 20 years, conservation efforts focused on the Sumatran tigers have increased, but the population continues to decline as a result of several key threats. To identify the status of the Sumatran tiger distribution across the island, an island-wide questionnaire survey comprised of 35 respondents from various backgrounds was conducted between May and June 2010. The survey found that Sumatran tigers are positively present in 27 habitat patches larger than 250 km(2) and possibly present in another 2. In addition, a review on major published studies on the Sumatran tiger was conducted to identify the current conservation status of the Sumatran tiger. Collectively, these studies have identified several key factors that have contributed to the decline of Sumatran tiger populations, including: forest habitat fragmentation and loss, direct killing of tigers and their prey, and the retaliatory killing of tigers due to conflict with villagers. The present paper provides management authorities and the international community with a recent assessment and a base map of the actual distribution of Sumatran tigers as well as a general overview on the current status and possible future conservation challenges of Sumatran tiger management.
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Prevalence of antibodies to type a influenza virus in wild avian species using two serologic assays
Article
Full-text available
  • Jul 2010
  • J WILDLIFE DIS
Serologic testing to detect antibodies to avian influenza (AI) virus has been an underused tool for the study of these viruses in wild bird populations, which traditionally has relied on virus isolation and reverse transcriptase-polymerase chain reaction (RT-PCR). In a preliminary study, a recently developed commercial blocking enzyme-linked immunosorbent assay (bELISA) had sensitivity and specificity estimates of 82% and 100%, respectively, for detection of antibodies to AI virus in multiple wild bird species after experimental infection. To further evaluate the efficacy of this commercial bELISA and the agar gel immunodiffusion (AGID) test for AI virus antibody detection in wild birds, we tested 2,249 serum samples collected from 62 wild bird species, representing 10 taxonomic orders. Overall, the bELISA detected 25.4% positive samples, whereas the AGID test detected 14.8%. At the species level, the bELISA detected as many or more positive serum samples than the AGID in all 62 avian species. The majority of positive samples, detected by both assays, were from species that use aquatic habitats, with the highest prevalence from species in the orders Anseriformes and Charadriiformes. Conversely, antibodies to AI virus were rarely detected in the terrestrial species. The serologic data yielded by both assays are consistent with the known epidemiology of AI virus in wild birds and published reports of host range based on virus isolation and RT-PCR. The results of this research are also consistent with the aforementioned study, which evaluated the performance of the bELISA and AGID test on experimental samples. Collectively, the data from these two studies indicate that the bELISA is a more sensitive serologic assay than the AGID test for detecting prior exposure to AI virus in wild birds. Based on these results, the bELISA is a reliable species-independent assay with potentially valuable applications for wild bird AI surveillance.
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Serum antibody titres to canine parvovirus, adenovirus and distemper virus in dogs in the UK which had been vaccinated for at least three years
Article
Full-text available
  • May 2004
Antibody titres to canine distemper (CDV), canine parvovirus (CPV) and canine adenovirus (CAV) were measured in 144 adult dogs that had not been vaccinated for between three and 15 years. Protective antibodies to CPV were present in 95 per cent of the population, to CDV in 71.5 per cent and to CAV in 82 per cent. The prevalence of protective titres did not decrease with increasing time interval from the last vaccination for any of the three diseases studied. Booster vaccination increased the dogs CAV titres. For comparative purposes, 199 puppies were sampled at the time of their first and second vaccination. In the case of CPV and CAV a significantly higher proportion of the adult dogs were protected than of the puppies immediately after they were vaccinated. Natural CPV boosting was strongly suspected because the dogs had significantly higher titres three years after their primary vaccination than two weeks after it and three unvaccinated dogs had acquired protective antibody levels uneventfully. There was no evidence of natural exposure to CDV.
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