Integrative Zoology 2015; 10: 329–343 doi: 10.1111/1749-4877.12137 1 ORIGINAL ARTICLE 1 2 2 3 3 4 4 5 5 6 Canine distemper virus as a threat to wild tigers in Russia and 6 7 7 8 across their range 8 9 9 10 1,2 1 3,4 5 10 11 Martin GILBERT, Svetlana V. SOUTYRINA, Ivan V. SERYODKIN, Nadezhda SULIKHAN, 11 12 Olga V. UPHYRKINA,5 Mikhail GONCHARUK,6 Louise MATTHEWS,2 Sarah CLEAVELAND2 12 13 1 13 14 and Dale G. MIQUELLE 14 15 1Wildlife Conservation Society, Bronx, New York, USA, 2Boyd Orr Centre for Population and Ecosystem Health, Institute of 15 16 Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, 16 17 Glasgow, UK, 3Pacifc Geographical Institute, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia, 17 18 18 4Far Eastern Federal University, Vladivostok, Russia, 5Institute of Biology and Soil Sciences, Far Eastern Branch of the Russian 19 19 6 20 Academy of Sciences, Vladivostok, Russia and Lazovskii State Nature Zapovednik , Lazo, Primorskii Krai, Russia 20 21 21 22 Abstract 22 23 23 Canine distemper virus (CDV) has recently been identifed in populations of wild tigers in Russia and India. Ti- 24 24 ger populations are generally too small to maintain CDV for long periods, but are at risk of infections arising 25 25 from more abundant susceptible hosts that constitute a reservoir of infection. Because CDV is an additive mor- 26 26 tality factor, it could represent a signifcant threat to small, isolated tiger populations. In Russia, CDV was asso- 27 27 ciated with the deaths of tigers in 2004 and 2010, and was coincident with a localized decline of tigers in Sikho- 28 28 te-Alin Biosphere Zapovednik (from 25 tigers in 2008 to 9 in 2012). Habitat continuity with surrounding areas 29 29 likely played an important role in promoting an ongoing recovery. We recommend steps be taken to assess the 30 30 presence and the impact of CDV in all tiger range states, but should not detract focus away from the primary 31 31 threats to tigers, which include habitat loss and fragmentation, poaching and retaliatory killing. Research prior- 32 32 ities include: (i) recognition and diagnosis of clinical cases of CDV in tigers when they occur; and (ii) collec- 33 33 tion of baseline data on the health of wild tigers. CDV infection of individual tigers need not imply a conserva- 34 34 tion threat, and modeling should complement disease surveillance and targeted research to assess the potential 35 35 impact to tiger populations across the range of ecosystems, population densities and climate extremes occupied 36 36 by tigers. Describing the role of domestic and wild carnivores as contributors to a local CDV reservoir is an im- 37 37 portant precursor to considering control measures. 38 38 39 Key words: canine distemper virus, conservation threat, extinction, Panthera tigris altaica, population decline 39 40 40 41 41 42 42 43 43 44 44 45 45 46 INTRODUCTION 46 47 47 Global populations of tigers, Panthera tigris (Linnae- 48 48 us, 1758), are at an all time low, with numbers of repro- 49 Correspondence: Martin Gilbert, Wildlife Conservation 49 ductive females in the wild dropping below 1000 indi- 50 Society, 2300 Southern Boulevard, Bronx, NY 10460, USA. 50 viduals (Walston et al. 2010). Pressure from agriculture, 51 Email: [email protected] 51 © 2015 International Society of Zoological Sciences, Institute of Zoology/ 329 Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd M. Gilbert et al. 1 industry and urbanization has fragmented tiger habitat, low et al. 2014). Infection of lymphatic cells, particu- 1 2 such that remaining populations occupy less than 7% larly T and B lymphocytes, and the severity of the re- 2 3 of their former range and more than half of the world’s sulting immunosuppression dictates the outcome of the 3 4 tigers are confined to habitat islands containing 25 or disease (Green & Appel 2006). By the second week of 4 5 fewer individuals (Sanderson et al. 2006; Walston et al. infection the virus spreads to epithelial cells, resulting 5 6 2010). Even in suitable habitat, tigers face a variety of in respiratory and gastrointestinal signs as well as vi- 6 7 threats, including competition with humans for prey re- ral shedding in the urine (Ludlow et al. 2014). The vi- 7 8 sources, direct poaching to meet the demand for their rus also enters the brain by crossing the blood–brain 8 9 body parts and retaliation due to conficts with humans barrier, or migrating along the olfactory nerve (Ludlow 9 10 (Walston et al. 2010; Chundawat et al. 2011). While et al. 2014). Many animals die during the initial stages 10 11 these anthropogenic factors are the main drivers of de- of the disease, but a proportion of the survivors may re- 11 12 clining tiger numbers (Robinson et al. 2015), these de- lapse some time later, with a progression of neurologi- 12 13 pleted populations face new pressures associated with cal signs (including behavioral changes, muscle twitch- 13 14 stochastic processes that have the potential to drive ing and seizures) as replication continues in the brain. 14 15 small, isolated populations to extinction. While inbreed- Dogs may continue to shed the virus for up to 60 days 15 16 ing depression is well recognized as a threat to small (Green & Appel 2006), but captive tigers have been re- 16 17 populations (Kenney et al. 2014), disease agents (patho- ported to shed the virus in urine for at least 150 days (V. 17 18 gens) can also be important drivers of stochastic extinc- Keahey 2014, pers. comm.), although this was based on 18 19 tion in carnivore populations (Thorne & Williams 1988; the results of molecular testing (reverse transcription 19 20 Timm et al. 2009); however, their potential impact on polymerase chain reaction [RT-PCR]), and therefore the 20 21 free-ranging tigers has received little research atten- presence of viable virus cannot be confirmed. Patho- 21 22 tion. In Russia, canine distemper virus (CDV) has re- logical lesions consistent with CDV infection were still 22 23 cently been recognized as a cause of death in Amur ti- present in a captive tiger with progressive neurological 23 24 gers, Panthera tigris altaica Temminck, 1844 (Quigley disease 18 months after initial exposure (Blythe et al. 24 25 et al. 2010; Seimon et al. 2013), and could pose a po- 1983), and may be analogous to ‘old dog syndrome’ de- 25 26 tential extinction threat, particularly to small popula- scribed in domestic dogs (Green & Appel 2006). 26 27 tions (Gilbert et al. 2014). Recent reports have also con- Most families within the order Carnivora are suscep- 27 28 frmed cases of CDV in wild tigers in India, indicating tible to CDV infection (Deem et al. 2000). However, the 28 29 that the threat may extend to tigers in other regions as severity of clinical disease varies widely, being largely 29 30 well (ProMED 2014). The objectives of the present pa- subclinical in some species (e.g. in domestic cats), while 30 31 per are: frst, to assess our current understanding of the causing severe systemic disease leading to high mortal- 31 32 status and impact of CDV on Amur tigers; second, to ity in others (e.g. ferrets) (Williams 2001). Clinical in- 32 33 consider the potential impact of CDV to tigers across fections and mortality have been recorded in a num- 33 34 their range; and third, to outline steps needed to assess ber of felids, but to date all published reports have been 34 35 and monitor the threat of CDV to tiger populations both within the genera of Panthera (including lion, tiger, 35 36 in Russia and elsewhere across their range. leopard, Panthera pardus, snow leopard, Panthera un- 36 37 cia, and jaguar, Panthera onca [Appel et al. 1994]) and 37 38 BIOLOGY OF CANINE DISTEMPER Lynx (including Canadian lynx, Lynx canadensis, Iberi- 38 39 an lynx, Lynx pardinus, and bobcat, Lynx rufus) (Daoust 39 40 VIRUS et al. 2009; Meli et al. 2010). Antibodies to CDV with- 40 41 Canine distemper is caused by a paramyxovirus out clinical disease or mortality have been reported in a 41 42 with a single-stranded RNA genome within the Mor- number of other cat species (including puma, Puma con- 42 43 billivirus genus, which has a near worldwide distribu- color, cheetah, Acinonyx jubatus, Geoffroy’s cat, Leop- 43 44 tion (Williams 2001; Green & Appel 2006). Transmis- ardus geoffroyi, and ocelot, Leopardus pardalis [Biek et 44 45 sion of CDV primarily occurs through the respiratory al. 2002; Munson et al. 2004; Fiorello et al. 2007; Dales 45 46 tract during close contact with an infected individual, Nava et al. 2008; Thalwitzer et al. 2010; Uhart et al. 46 47 but quantities of the virus are also shed in the urine and 2012]), suggesting that susceptibility may vary within 47 48 feces. The virus generally enters the body via the respi- the Felidae. This is supported by the low competence of 48 49 ratory tract by infecting alveolar macrophages, and then domestic cats as CDV hosts during experimental stud- 49 50 spreads rapidly throughout the lymphatic system (Lud- ies (Appel et al. 1974), and relates to differences in the 50 51 51 330 © 2015 International Society of Zoological Sciences, Institute of Zoology/ Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd Canine distemper virus in tigers 1 structure of the cellular receptor (CD-150 or signaling The multi-host nature of CDV represents a particu- 1 2 lymphocyte activation molecule [SLAM]) used by CDV lar threat to endangered populations in situations where 2 3 to enter lymphoid cells (Ohishi et al.