Canine Distemper Virus As a Threat to Wild Tigers in Russia and Across

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

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

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. 2014). Clinical in- they coexist with more abundant susceptible hosts, 3 4 fections and mortality have also been recorded in other which can act as a reservoir of infection (see Fig. 1). 4 5 taxa, including rodents (Origgi et al. 2013), nonhuman The fortunes of many single-host pathogens are den- 5 6 primates (Yoshikawa et al. 1989; Sun et al. 2010) and sity-dependent, where a decline in host density (e.g. 6 7 peccaries (Appel et al. 1991). through infection-related mortality) leads to a reduced 7 8 8 9 9 10 10 11 11 12 12 13 Taken in isolation, populations of endangered species, such as tigers, are generally too small and at too low a density to maintain ca- 13 14 nine distemper virus (CDV) in the long term. These populations fall below a critical community size (CCS), beneath which a patho- 14 15 gen is unable to persist due to a depletion of susceptible hosts over time (Bartlett 1960). Multi-host pathogens, such as CDV, may 15 16 represent a persistent threat to small populations, through regular spillover transmission from a pathogen reservoir. In the face of 16 17 such complexity, a framework proposed by Haydon et al. (2002) for describing the constituents of a reservoir system provides a 17 18 useful basis for understanding its functional dynamics. This defnes a reservoir as one or more epidemiologically connected popu- 18 19 lations in which the pathogen can be permanently maintained and from which infection is transmitted to the defned target species 19 20 (e.g. tigers). Individual populations that exceed the CCS, and can, therefore, maintain infection indefnitely are termed maintenance 20 21 populations, although several non-maintenance populations could act synergistically to form a maintenance community. Finally, a 21 source population is that which transmits infection directly to the target, and may either be a maintenance population, or be connect- 22 22 ed to the maintenance population as a transmission link to the target. 23 23 The structure and constituent populations within a CDV reservoir are likely to vary across the global tiger range depending on the 24 24 diversity, density and demography of susceptible host species. In Russia, reservoir candidates include domestic dogs and abundant 25 25 wild carnivores, including sable (Martes zibellina), red fox (Vulpes vulpes), raccoon dog (Canis lupus familiaris) and Eurasian bad- 26 26 ger (Meles meles). Two simplistic representations of possible reservoir structures in Russia are illustrated in diagrams A and B. 27 27 28 28 29 29 30 30 31 31 32 32 33 33 34 34 35 35 36 36 37 37 38 38 39 39 40 Populations can either be maintenance populations (squares) or non-maintenance populations (circles). Transmission of CDV oc- 40 41 curs in the direction indicated by the arrows. In A, dogs (d) and sable (s) exceed the CCS and are maintenance populations, while 41 only raccoon dogs (rd) and dogs act as source populations of CDV infection for tigers (t). In this case all 3 populations contribute to 42 42 the reservoir (indicated in grey), and control measures would need to target both transmission from dogs and raccoon dogs to tigers. 43 43 In B, no individual population exceeds the CCS, but transmission between raccoon dogs and sable is such that the 2 populations can 44 44 form a maintenance community (represented by the black frame). In this case raccoon dogs represent the only source of infection 45 45 for tigers, and control measures would need to target either one or both of the populations contributing to the maintenance commu- 46 nity, +/or the transmission of virus from raccoon dogs to tigers. Clearly, these are just examples, and many other possible combina- 46 47 tions exist. However, successful control of CDV requires management of infection in maintenance populations or communities and/ 47 48 or their transmission linkages with the tiger population. 48 49 49 50 50 51 Figure 1 Defning the canine distemper virus reservoir. 51

1 opportunity for infection. By contrast, more cosmopol- ca-2 and Asia-1 clades) (Appel et al. 1994; Nagao et al. 1 2 itan multi-host pathogens may continue to infect rare 2012; Seimon et al. 2013). 2 3 host species in areas where a reservoir continues to act 3 4 as a source of the virus, even as the endangered popu- CANINE DISTEMPER VIRUS IN AMUR 4 5 lation declines. Outbreaks of CDV have been implicat- 5 6 ed in population declines and near extinction of several TIGERS 6 7 7 wildlife species, including the African wild dog, Lycaon Comparatively more is known about the health of 8 8 pictus (Fanshawe et al. 1991), the Santa Catalina Island 9 wild tigers in Russia than any other range country, as 9 10 fox, Urocyon littoralis catalinae (Timm et al. 2009), samples are routinely collected whenever live or dead 10 11 and the black-footed ferret, Mustela nigripes (Thorne & tigers are handled. Serum collected from tigers im- 11 12 Williams 1988). mobilized during the placement of telemetry collars 12 13 Even in susceptible species, the epidemiology of and in response to tiger–human confict situations pro- 13 14 CDV can be complex. For instance, CDV has been im- vides a baseline for assessing pathogen exposure (Go- 14 15 plicated in local population declines of lions and African odrich et al. 2012; Naydenko et al. 2012). No CDV an- 15 16 wild dog in several areas in East Africa (Fanshawe et al. tibodies were detected in 27 tigers sampled from 1992 16 17 1991; Roelke-Parker et al. 1996). However, in southern to 1999, suggesting that tigers at this time were not ex- 17 18 Africa, populations of these species have remained sta- posed to the virus (Goodrich et al. 2012). However, Go- 18 19 19 ble, despite high levels of CDV exposure (Alexander et odrich et al. (2012) report antibodies to CDV in 6 of 20 20 al. 2010). Alexander et al. propose that habitat hetero- 13 tigers captured between 2000 and 2004, suggesting 21 21 the introduction of CDV into this population during the 22 geneity in southern regions led to a more complex host 22 early 2000s. In November 2003, a tigress captured in 23 population structure, limiting the spread of outbreaks 23 24 and enabling recolonization from surrounding areas the village of Pokrovka, Khabarovskii Krai (46.69°N, 24 25 in the wake of local extinctions. However, even in the 134.03°E) was taken into care but died fve weeks later 25 26 more homogeneous grassland environments of East Af- (Quigley et al. 2010). Although ambulatory at the time 26 27 rica, CDV-induced losses are not inevitable, with mul- of capture, this tigress was non-responsive to stimuli 27 28 tiple waves of CDV exposure evident in the serology and unafraid of humans. She was later confrmed as the 28 29 profles of the lion populations without coincident sick- frst case of CDV in a wild tiger (Seimon et al. 2013). 29 30 ness or population impact (Munson et al. 2008; Viana et Further cases of CDV in Amur tigers were con- 30 31 al. 2015). Overt outbreaks among the lions of Serenge- firmed in 2010. These included a 3–4-year-old male 31 32 ti in 1994 and Ngorogoro in 2001 were attributed to cli- captured near the village of Aleksayevka, Primorskii 32 33 33 matic patterns resulting in high vector numbers, with Krai (43.56°N, 132.00°E) during February 2010, and an 34 34 mortality from CDV associated with Babesia infection 8.5-year-old tigress who entered the village of Ternei, 35 35 loads (Munson et al. 2008). The involvement of viral 36 Primorskii Krai (45.04°N, 136.78°E) and was shot on 36 37 co-infections has been implicated in other cases of CDV 1 June 2010 (Seimon et al. 2013). A third case in 2010 37 38 mortality (Fix et al. 1989; Burtscher & Url 2007; Orig- has recently been confirmed based on sequences ob- 38 39 gi et al. 2013), and, therefore, it is important to consid- tained from archived tissues and involved an adult male 39 40 er these, or other physiological stressors as a precur- tiger that was shot close to Ternei in January 2010 (Gil- 40 41 sor to disease. In spite of this, apparently uncomplicated bert et al. 2014, unpubl. data). All of these animals dis- 41 42 CDV infections have led to mortality in captive tigers in played neurological signs and were unafraid of humans. 42 43 North America, Europe and Asia, and so it appears that Video footage of a tiger behaving in this characteristic 43 44 clinical outcome is not always dependent on co-infec- manner was taken along the Vladivostok-Khabarovsk 44 45 tions (Appel et al. 1994; Nagao et al. 2012; Seimon et highway between the towns of Vyazemski and Bikin, 45 46 al. 2013). This may be due to variation in the virulence Khabarovskii Krai during the spring of 2010 (http://ti- 46 47 of different CDV strains, although it should be not- nyurl.com/las2yt7). Although this animal later died in 47 48 48 ed that genetically diverse strains have caused mortal- care, no samples were available for analysis; therefore, 49 49 ity in Panthera species without apparent co-infections CDV could not be confrmed in this case. 50 50 51 (including viruses from the Arctic-like, North Ameri- 51

1 CANINE DISTEMPER VIRUS IN 2010) and a small number of isolated dwellings lie out- 1 2 side the protected area and represent a source of contact 2 3 SIKHOTE-ALIN BIOSPHERE for tigers with territories along the reserve boundary, as 3 4 ZAPOVEDNIK well as individuals without territories that may move 4 5 more widely through the landscape. 5 One of the most closely monitored populations of 6 One of the confirmed CDV cases in 2010, the 6 Amur tigers inhabits the Sikhote Alin Biosphere Zapov- 7 8.5-year-old tigress known as T02 (referred to as Pt 7 ednik (SABZ) in Primorskii Krai. The reserve is of suf- 8 2010-3 in Seimon et al. 2013), held a territory along 8 9 ficient size to hold territories for 11 breeding females 9 2 the southern border of SABZ (Figs 2a and 3). This ti- (assuming a territory of 384 km , with average over- 10 gress had been captured in 2002 and 2005 as part of a 10 11 lap of 11% between adjacent female territories) and 4 11 2 telemetry study, yet no CDV antibodies were detect- breeding males (assuming a territory of 1160 km , with 12 ed from routine samples. She was subsequently recap- 12 average overlap of 14% between adjacent male territo- 13 tured on 24 March 2010, by which time CDV antibod- 13 ries), and lies within a wider matrix of suitable habitat 14 ies were circulating (with a virus neutralization titre of 14 that enables tigers to disperse to and from surrounding 15 1:256 measured at the Washington Animal Disease Di- 15 areas. This protected area limits access, allowing only 16 agnostic Laboratory, Pullman, WA, USA). In view of 16 rangers and researchers, such that tigers in core areas 17 subsequent events, and the strong protective immuni- 17 may rarely, if ever, encounter humans. However, four 18 ty that develops in animals that survive infection, it is 18 villages (inhabited by between 67 and 5350 people in 19 likely that T02 was already infected by March 2010. 19 20 20 21 21 22 22 23 23 24 a b 24 25 25 26 26 27 27 28 28 29 29 30 30 31 31 32 32 33 33 34 34 35 35 36 36 37 37 38 38 39 39 40 40 41 41 42 42 43 43 Figure 2 (a) Locations of resident female tigers in Sikhote-Alin Biosphere Zapovednik (dark grey). Map includes rivers (black 44 44 lines) and roads (double lines). Tigresses are illustrated by circles, and include T02 (red), T5 (blue), T6 (yellow), T7 (green), T14 45 (purple) and T21 (white). Locations refer to camera trap captures made during 2009 and 2010, with the exception of T14, where 45 46 captures from 2007 and 2008 are used (as this tiger was not photographed in 2009 or 2010). The home range of a further tigress (T47) 46 47 is represented using a minimum convex polygon (orange), based on telemetry positions obtained during November and December 47 48 2009. (b) Locations of resident male tigers in Sikhote-Alin Biosphere Zapovednik (dark grey). The map includes rivers (black lines) 48 49 and roads (double lines). Tigers are illustrated by triangles, and include T10 (green), T15 (yellow), T16 (red), T19 (white) and T27 49 50 (blue). Locations refer to camera trap captures made during 2009 and 2010, with the exception of T10, T15 and T19, where captures 50 51 from 2007 and 2008 are used (as these tigers were not photographed in 2009 or 2010). 51

1 Tiger ID Estimated Date of last 1

2 2010 2

number year of birth Sex Status record 2006 2007 2008 2009 2011 2012 Outcome 3 T02 2001 F R 1 June 2010 Mortality (CDV confrmed) 3 4 T03 ~1992 F R 2007 Mortality (poached) 4 5 T04 ~1998 M R 2007 Mortality (poached) 5 T05 2001 F R 27 October 2009 Mortality (unexplained)† 6 1 November 6 7 T06 2004 F R 2009 Disappeared (unexplained) 7 8 6 November 8 9 T07 UNK F R 2009 Disappeared (unexplained) 9 10 T08 2006 F DC 2008 Dispersed to North SABZ 10 6 December 11 T09/PT85 UNK M R 2007 Mortality (unexplained) 11 12 T10 UNK M R 2007 Disappeared (unexplained) 12 13 T14 UNK F R Alive 2013 Alive (circa 2013) 13 14 T15 UNK M R 2007 Disappeared (unexplained) 14 15 T16/PT90 ~1999 M R January 2010 Mortality (CDV confrmed) 15 16 November 16 T17/PT80 2005 F R 2007 Mortality (poached) 16 17 T18/PT89 2006 M DC 30 July 2008 * Disappeared (dispersed?) 17 18 T19 UNK M R February 2011 > Mortality (natural)‡ 18 8 December 19 * 19 20 T20 2006 F DC 2008 Disappeared (dispersed?) 20 T21 UNK F R 13 April 2011 > Disappeared (unexplained) 21 22 September 21 * 22 T25/PT88 2006 M DC 2008 Emigrated from SABZ 22 23 T26/PT35 1993 F R 2007 Disappeared (unexplained)§ 23 24 T27 UNK M R Alive 2013 > Alive (circa 2013) 24 T29/PT96 2008 M DC 17 January 2010 * Disappeared (dispersed?) 25 T05 Cub A 2008 UNK DC 2009 * Disappeared (unexplained) 25 26 T05 Cub B 2008 UNK DC 2009 * Disappeared (unexplained) 26 27 11 December 27 * † 28 T47/PT97 2008 F R 2009 Mortality (unexplained) 28 T30 UNK M R Alive 2013 > Alive (circa 2013) 29 29 T32/PT100 2006/07 M R December 2011 > Mortality (poached) 30 T02 Cub A 2010 F DC May 2010 * Mortality (CDV related) 30 31 T02 Cub B 2010 F DC May 2010 * Mortality (CDV related) 31 32 T02 Cub C 2010 F DC May 2010 * Mortality (CDV related) 32 33 T33 2010/11 F DC December 2011 * Disappeared (dispersed?) 33 34 T34 2010/11 M DC December 2011 * Disappeared (dispersed?) 34 2010 * ¶ 35 T21 Cub A UNK DC 2011 Mortality (natural) 35 T21 Cub B 2010 UNK DC 2011 * Mortality (natural)¶ 36 36 T35/PT114 2009 F R Alive 2013 > Alive (circa 2013) 37 T35 Cub A 2012 UNK DC Alive 2013 * Alive (circa 2013) 37 38 T35 Cub B 2012 UNK DC Alive 2013 * Alive (circa 2013) 38 39 T35 Cub C 2012 UNK DC Alive 2013 * Alive (circa 2013) 39 8 November 40 > †† 40 PT95 2004 M UNK 2009 Disappeared (dispersed?) 41 41 42 Figure 3 A summary of camera trap captures of tigers in the central and southern regions of Sikhote Alin Biosphere Zapovednik 42 43 (SABZ) between 2006 and 2013. Details of individual tigers include identity code, estimated year of birth, sex (F = female, M = 43 44 male, UNK = unknown), status (R = resident, DC = dependent cub), the date and circumstances of last sightings. Identifers with 44 45 the prefx T refers to tigers recorded by camera trap, and the prefx PT refers to tigers ftted with radio collars. Both systems are 45 46 used here to facilitate comparison with other publications. Transient tigers (recorded in only a single year) are excluded, as out- 46 47 come could not be determined. Annual status of each tiger is indicated for animals captured at least once (dark green), not captured 47 and presumed absent (yellow), not captured but subsequently confrmed (light green), or not surveyed for (grey). The timing of 48 48 births are indicated by blue asterisks, and confrmed tiger deaths are indicated by cells outlined in red. Additional notes on the cir- 49 49 cumstances of tiger deaths and disappearances are provided as footnotes. The arrival of immigrants is indicated using blue arrows. 50 (†Scavenged/predated by large carnivore. ‡Killed by another tiger. §Likely old age [14 years]. ¶Killed by T19. ††Possible transient. 50 51 CDV, canine distemper virus. 51

1 Antibodies to CDV appear after 10 to 20 days post-in- played an unusual lack of fear, remaining in the open 1 2 fection in dogs (Green & Appel 2006), which if com- until he was shot and killed the following day. T16 was 2 3 parable in tigers would suggest an infection lasting at recorded in association with T02 in the fall of 2009. As- 3 4 least 80 to 90 days in this tigress. By 1 May, T02 local- suming that T16 had sired the litter of T02, then mating 4 5 ized her movements, and (as was later confrmed) gave must have occurred just a few days prior to his death 5 6 birth to a litter of three cubs. Although T02 had proven (given a gestation period of 98–111 days [Wack 2003]). 6 7 to be a typically attentive mother when raising her three In captive tigers mortality from CDV usually occurs 7 8 prior litters, on this occasion her behavior was unusual, within days or weeks of developing clinical signs (Gould 8 9 leaving the den for several days at a time before fnally & Fenner 1983; Appel et al. 1994; Konjevic et al. 2011; 9 10 abandoning her cubs entirely on 17 May. She was sub- Nagao et al. 2012; V. Keahey, pers. comm.), but the 10 11 sequently observed at a nearby military outpost, before length of the refractive period (before clinical disease is 11 12 12 entering Ternei, where she was shot on 1 June 2010 to evident) remains unknown, and a delayed onset may be 13 13 prevent injury to local residents. The presence of CDV possible (Blythe et al. 1983). Therefore, it is conceiv- 14 was confrmed in brain tissue collected from T02, by se- 14 able that T02 contracted her infection through contact 15 quencing of amplifed gene products, and demonstration 15 with T16. 16 of consistent pathology (Seimon et al 2013). All three 16 The deaths of T16, T02 and her 3 cubs coincided 17 of her cubs consequently died. Evidence of CDV was 17 with a period of heavy losses for the SABZ tiger pop- 18 not found in samples collected from 1 of those cubs, al- 18 ulation (Fig. 3). Population estimates for the whole of 19 though decomposition may have hampered test sensitiv- 19 SABZ based on snow tracking data indicated a decline 20 ity. 20 from 25 tigers in 2008 to 9 by 2012 (Fig. 4). Camera 21 A recent re-examination of tissues collected from an- 21 22 trap surveys carried out in the central and southern sec- 22 other SABZ tiger, T16 (referred to as Pt 2010-1 in Sei- 23 tions of SABZ provide a more detailed account of the 23 mon et al. 2013) has confirmed that he was infected 24 numbers and movements of a subset of the reserve’s ti- 24 with CDV at the time of death (Gilbert et al. 2014, un- 25 gers, and highlight a similar decline (Fig. 3 [Soutyri- 25 publ. data, Fig. 3). This tiger was an 11-year-old male, 26 na et al. 2013]). The population of 15 tigers identifed 26 who occupied a territory that encompassed that of T02. 27 on camera traps in 2008 (representing a minimum pop- 27 On 31 December 2009, T16 approached and killed a lo- 28 ulation) had declined to 7 identifed by the start of 2011 28 cal fisherman close to a group of houses 10 km west 29 (Table 1). Determining the cause of death in cryptic spe- 29 30 of Ternei. In common with other CDV cases, T16 dis- 30 31 31 32 32 33 33 34 34 35 35 36 36 37 37 38 38 39 39 40 40 41 41 42 42 43 43 44 44 45 45 46 46 47 47 48 48 49 49 50 Figure 4 Annual tiger population estimates based on snow track surveys of Sikhote-Alin Biosphere Zapovednik from 1962 to 2012. 50 51 Surveys are conducted annually from December through February along transects throughout the entire reserve. 51

1 Table 1 Population demographics of tigers in Sikhote-Alin Biosphere Zapovednik based on camera trapping surveys of central and 1 2 southern regions of the reserve during 2006–2013. Numbers represent minimum estimates based on individual identifcations of all 2 3 tigers captured during camera trap surveys 3 4 Tigers at year 4 5 Year start (minimum) Immigrants Births Deaths Disappear Emigrants Transient 5 6 6 2006 ? 0 1 ? ? ? 4 7 7 8 2007 14 1 3 3 0 0 0 8 9 2008 15 2 2 2 3–5 2 0 9 10 2009 10–12† 1 2 3 0–2 0 1 10 11 2010 10 1 5 6 3 0 0 11 12 12 2011 7 2 2 3 0 0 1 13 13 14 2012 8 1 3 1 3 0 1 14 15 2013 8 4 8 ? ? ? 0 15 16 “Deaths” refers to confrmed mortalities (e.g. where a body was recovered, or intelligence indicated a poaching incident), “Disap- 16 17 pear” indicates absence of tigers where cause is unknown. †Two tigers (T10 and T15) disappeared some time during the years 2008 17 18 and 2009. However, no camera traps were set within their territories during this period to confrm the timing of their disappearance. 18 19 For this reason a range of values is used to express the minimum number of tigers present at the start of 2009. 19 20 20 21 21 22 22 23 23 24 24 25 25 26 26 27 27 28 28 29 29 30 30 31 31 32 32 33 33 34 34 35 35 36 36 37 37 38 38 39 39 Figure 5 Annual tiger mortality and disappearances in Sikhote-Alin Biosphere Zapovednik between 2006 and 2012 attributed to 40 40 poaching (white), canine distemper virus (CDV)-related (black), dispersal (confrmed or suspected based on disappearance at an age 41 41 appropriate for dispersal [light gray]), natural (confrmed mortalities unrelated to humans and excluding CDV-related [cross hatch] 42 42 and unexplained [dark grey]). 43 43 44 44 45 45 46 46 cies like tigers can be challenging, particularly in remote During late 2009 a resident adult tigress (T05, Fig. 3) 47 47 areas such as SABZ. However, the unexplained death or was found dead, with no sign of her litter of 2 or more 48 48 disappearance of 6 tigers during 2009 was unusual (Fig. dependent cubs (although at approximately 1.5 years of 49 49 5), and it is possible that several of these may have been age these tigers may have dispersed beyond the study 50 50 related to CDV infections that were undetected. area). The body of a second younger tigress (T47) was 51 51

1 found several months later (Fig. 3). Both of these car- frmed and suspected cases of CDV in 2010 occurred in 1 2 casses had been eaten by a bear or other large carni- disparate locations 300–500-km apart, near human habi- 2 3 vore, although it was unclear whether this was the result tation and in distant corners of the Amur tiger’s range. It 3 4 of predation or scavenging. Consequently, the cause of is unknown whether the proximity of these tigers to hu- 4 5 death in these cases is open to speculation, and it is like- man habitation increased opportunities to contract CDV, 5 6 ly that a young newly independent tigress such as T47 or merely the chance that cases would be reported. 6 7 could have succumbed to any of a number of possible However, with the majority of Amur tigers occupying 7 8 dangers. However, T05 shared a territory with T16, the vast, largely uninhabited areas, it is possible that oth- 8 9 likely father of her cubs (Fig. 2), as did another resident er tigers may have succumbed to CDV during the 2009– 9 10 adult tigress (T07) that was last recorded by camera trap 2010 period without detection. Yet with so many un- 10 11 on 6 November 2009 (Figs 2 and 3). A neighboring ti- certainties relating to the epidemiology of CDV across 11 12 gress (T06) also disappeared in late 2009, with the last the Amur tiger range, there is a limit to the inferences 12 13 camera trap record on 1 November 2009 (Fig. 3). Mor- that can be drawn from the SABZ outbreak, and the ex- 13 14 talities unrelated to CDV continued in early 2011, with tent to which the overall Amur tiger population may 14 15 the death of 2 dependent cubs attributed to infanticide have been affected. Under these circumstances, popula- 15 16 carried out by an adult male (T19), who also succumbed tion modeling can be a valuable tool to explore the key 16 17 soon after to injuries sustained in a fght with another ti- determinants that infuence the impact of CDV on tiger 17 18 ger (Fig. 3). In May 2011, the carcass of a female with populations. Recent models have shown that even mod- 18 19 enlarged nipples (which suggested she was still nursing est levels of tiger contact with a CDV reservoir will im- 19 20 a litter) was found with 2 bullet wounds (This tiger was pact population growth, and that small and isolated ti- 20 21 not captured or recorded on camera traps, and so is not ger populations are disproportionately impacted (Gilbert 21 22 included in Table 1). et al. 2014). Refnements of models such as this require 22 23 These results suggest that there were multiple caus- a more detailed understanding of reservoir composition 23 24 es of death occurring in the SABZ population within a and dynamics, if they are to provide further insights into 24 25 small (18-month) timeframe (late 2009–early 2011) (Fig. the threat to a particular tiger population. 25 26 3). CDV was not solely responsible for the dramatic de- 26 27 clines in SABZ tigers during 2009 and 2010, but in a UNDERSTANDING RESERVOIR 27 28 worse case scenario (including the unknown causes that 28 29 might have been disease-related) it is possible that as STRUCTURE 29 30 many as 6 adults/subadults succumbed to the virus, and An understanding of local reservoir structure is a crit- 30 31 at least 1 litter of 3 was lost because their mother was ical frst step to begin assessing the impact that a multi- 31 32 diseased. This additive mortality factor (Robinson et al. host pathogen will have on a population, and is an 32 33 2015) demonstrates the vulnerability of small tiger pop- important precursor to the design of management prac- 33 34 ulations to stochastic events. The SABZ population has tices. Defning a reservoir is complex, but a framework 34 35 benefted from the continuity of habitat, which has en- proposed by Haydon et al. (2002, and summarized in 35 36 abled immigration of tigers from surrounding areas, and Fig. 1) provides a useful means of conceptualizing al- 36 37 with continued protection and successful reproduction, ternative structures. All populations of tigers share hab- 37 38 recovery is already occurring (a minimum of 20 tigers itat with a number of susceptible species that could con- 38 39 were recorded by winter 2014). For smaller tiger popu- tribute to the local CDV reservoir as maintenance or 39 40 lations, or those that are more isolated, the likelihood of non-maintenance hosts depending on their susceptibili- 40 41 withstanding additive losses similar to those occurring ty, population size, turnover and frequency of effective 41 42 in SABZ during 2009 and 2010 would be considerably contacts. More abundant susceptible hosts are likely to 42 43 lower. have a greater contribution to CDV maintenance, and in 43 44 44 The close monitoring of tigers in SABZ enables a de- the context of the Russian Far East this is likely to in- 45 45 tailed reconstruction of individual life histories of the ti- clude domestic dogs, and small or medium-bodied wild 46 46 ger population during the period that CDV was circulat- carnivores, particularly raccoon dogs, Nyctereutes pro- 47 47 ing in 2009 and 2010. However, even in this intensively cyonoides, red foxes, Vulpes vulpes, Eurasian badgers, 48 48 monitored sub-population we are limited to best-guess Meles meles, and sable, Martes zibellina. Tigers prey on 49 49 estimates of the impact that CDV had on the tiger pop- each of these host species, providing a likely route for 50 50 ulation in the reserve. Beyond SABZ, tigers with con- CDV transmission (Miquelle et al. 1996; Ludlow et al. 51 51

1 2014). Underscoring this potential route of exposure, ki 1990), and as CDV is shed in both feces and urine, 1 2 rangers in SABZ reported mortalities of red foxes and and as the virus has a half life of 9–11 days at 4°C (Appel 2 3 raccoon dogs from an unidentifed disease in both 2009 1987), contaminated carcasses could remain infectious 3 4 and 2010. Although tigers are largely solitary, they do for an extended period. A similar mechanism could fa- 4 5 interact regularly, albeit infrequently, providing a poten- cilitate indirect transmission between tigers, through use 5 6 tial mechanism for tiger-to-tiger transmission (Goodrich of urine scent marks on trees and landmarks that are reg- 6 7 et al. 2010). Aside from contact between mother and ularly visited by territorial tigers of both sexes, as well 7 8 cubs, intra-specific contact is likely to be greatest be- as non-territory holders that may be passing through. 8 9 tween territorial tigers of the opposite sex, and in Rus- Although other carnivore species represent the most 9 10 sia these contacts occur around 1 or 2 times per month likely source of CDV infection for tigers, it should be 10 11 (Goodrich et al. 2010). In other tiger populations where noted that the virus has been associated with infections 11 12 tigers occupy smaller home ranges, and occur in high- in non-carnivores, including Artiodactyls (Appel et al. 12 13 er densities, these interactions are likely to be more fre- 1991; Noon et al. 2003; Kameo et al. 2012). An out- 13 14 quent, potentially increasing the rate of tiger-to-tiger break of CDV in collared peccaries, Tayassu tajacu, in 14 15 transmission. Arizona was associated with high mortality (Appel et al. 15 16 In the Russian Far East domestic dogs occur at com- 1991), and the virus was found to be common and enzo- 16 17 paratively low densities compared to other parts of the otic in the population (Noon et al. 2003). While such a 17 18 world. Due to harsh climatic conditions, feral dog pop- severe clinical syndrome has not been recorded in oth- 18 19 ulations are almost non-existent, with most animals re- er ungulates, viraemia has been demonstrated in domes- 19 20 lying on provisioning by humans for survival. Based on tic pigs following experimental exposure (Appel et al. 20 21 2010 census data there were almost 2 million people in 1974), and antibodies to CDV (indicating prior expo- 21 22 Primorskii Krai, of which more than 75% resided in ur- sure) were found in 11/41 wild boar, Sus scrofa, and 2/5 22 23 ban centers and were, therefore, unlikely to come into sika deer, Cervus nippon, tested in Japan (Kameo et al. 23 24 contact with tigers. The remaining population is sparse- 2012). Amur tigers prey on boar or deer with far greater 24 25 ly distributed across the landscape, at mean densities as frequency than carnivore species. While these ungulates 25 26 low as 2.83 people/km2. Based on preliminary estimates may be unlikely contributors to a reservoir, they could 26 27 of human : dog ratios, this would equate to a mean den- enhance effective contact between tigers and the reser- 27 28 sity of approximately 5.10 dogs/km2, dramatically lower voir. A potential scenario could arise if wild boar were 28 29 than the dog density of 719 dogs/km2 recorded in Ma- to contract subclinical infections when scavenging the 29 30 harashtra, India (Belsare & Gompper 2013), suggesting carcasses of infected carnivores, and transmit the virus 30 31 that the contribution of domestic dogs to the CDV res- when subsequently predated by a tiger. Such a scenario 31 32 ervoir may be much more important in other parts of the remains unsubstantiated, but worthy of study. 32 33 tiger range. 33 34 POTENTIAL CONTROL MEASURES 34 35 OTHER FACTORS POTENTIALLY 35 36 Options for managing the impact of CDV infections 36 37 INFLUENCING CANINE DISTEMPER on tiger populations will depend on the structure of the 37 38 VIRUS ECOLOGY IN RUSSIA local reservoir, the mechanism of viral maintenance and 38 39 the source of infection for the tigers. Intervention strat- 39 40 Due to the relative fragility of CDV virion to envi- egies for managing disease in wildlife are often expen- 40 41 ronmental conditions (e.g. heat, desiccation and ultravi- sive, and so it is important that control measures are 41 42 olet radiation), transmission is typically thought to re- weighed against the risk that CDV represents to the ti- 42 43 quire close contact between infected individuals (Green ger population, are kept proportional and are achievable 43 44 & Appel 2006). However, considering the extreme cold (Woodroffe 1999). In principal, potential management 44 45 of the Russian winter, viability could be prolonged, with strategies could be directed at the control of disease in 45 46 the virus persisting for extended periods outside the the target tiger population, at blocking transmission be- 46 47 host, raising the potential for indirect modes of trans- tween the target and source population, or at the mainte- 47 48 mission. Most local carnivore species will scavenge nance population(s) that contribute to the virus reservoir 48 49 from carcasses in the forest, including tiger kills. Sev- (Haydon et al. 2002). Each of these strategies requires 49 50 eral carnivores, particularly canids, are known to scent progressively more understanding of the reservoir struc- 50 51 mark, urinate or defecate on or around food (Goszcyns- ture to ensure confdence of success. 51

1 Strategies directed at target populations could theo- are more likely to have encountered the virus, and may 1 2 retically include treatment of infected individuals or im- be less important to CDV circulation (Belsare 2013). 2 3 munization (Woodroffe 1999). At present, antiviral ther- Reduction of dog populations through responsible own- 3 4 apies are of limited use in treating CDV, although the ership combined with vaccination of puppies might have 4 5 development of pharmaceuticals that block the RNA the greatest chance of success. However, in situations 5 6 polymerase enzymes utilized during CDV replication where wildlife are important contributors to CDV, main- 6 7 could lead to applications in the treatment of affected tenance control will be extremely diffcult, as the lack of 7 8 individuals (Krumm et al. 2014). This is unlikely to rep- an oral vaccine, and low effcacy and ethical issues as- 8 9 resent a solution in the Russian context, where there is sociated with wildlife population control prohibit man- 9 10 a low probability of encountering infected tigers, but agement of CDV in a wild reservoir (Woodroffe 1999). 10 11 could be considered in higher density populations that 11 12 can be monitored more closely. CRITICAL STEPS NEEDED TO ASSESS 12 13 Contemporary vaccines fall into two main catego- 13 14 ries: modified live vaccines (MLV [grown on canine AND MONITOR THE THREAT OF 14 15 or avian kidney cell lines]); and recombinant vaccines CANINE DISTEMPER VIRUS 15 16 that use a canarypox vector to present CDV antigens to 16 17 the immune system. Each of these has innate advantag- As CDV is known from all countries where tigers oc- 17 18 es and disadvantages. While MLVs can induce a strong cur, the virus represents a potential threat to wild tigers 18 19 and long-lasting immunity in many species, older MLVs throughout their range. While the diversity of CDV sus- 19 20 (particularly those derived from canine cell culture such ceptible hosts may vary across tiger range countries, 20 21 as Rockborn or Snyder Hill strains) can cause sickness abundant populations of domestic dogs and/or wild car- 21 22 and death in select taxa (McCormick 1983; Montali et nivores, acting alone or in concert, could represent a 22 23 al. 1983). New generation MLVs have been used suc- CDV reservoir, and source of infection for tigers. Wild- 23 24 cessfully in a limited trial in lions (Kock et al. 1998), life managers and veterinarians in tiger range coun- 24 25 and offer potential for use in tigers. However, it would tries should be encouraged to introduce the following 25 26 be important to verify their safety and immunogenicity measures as a frst step to assess the risk that CDV rep- 26 27 in captive tigers before their use was proposed in a wild resents for their tiger populations: 27 28 population. Recombinant vaccines are safer, but produce 1. Recognize and diagnose clinical cases of CDV in ti- 28 29 a less pronounced immune response that requires multi- gers when they occur: CDV should be considered among 29 30 ple doses to induce life-long immunity. One major dis- the differential diagnoses for any tiger that displays be- 30 31 advantage of both vaccine classes is that they are only havioral or neurological abnormalities. Previous cas- 31 32 available in injectable form, presenting a major chal- es of CDV in tigers have presented with some or all of 32 33 lenge for delivery to most free-ranging tigers. the following: fearlessness, sensory defcits (e.g. blind- 33 34 34 Strategies to block transmission from the reservoir ness), ataxia and or muscular tremors, as well as gener- 35 35 to tiger populations are limited, particularly if wildlife al poor body condition. Behavioral changes, particular- 36 36 constitute an important source of infection. Measures to ly loss of fear, may predispose animals to situations of 37 37 reduce dog predation, such as preventing access to tiger human–tiger confict. Suspected cases can be confrmed 38 38 habitat, could be benefcial in theory, but are unlikely to through detection of genetic sequences specifc to CDV 39 39 be socially acceptable where licensed hunters extensive- (e.g. using RT-PCR or equivalent techniques). Post mor- 40 40 ly use dogs, as they do in the Russian Far East. tem samples such as brain tissue has the greatest diag- 41 nostic value during the later stages of infection when 41 Attempts to control CDV in the reservoir require a 42 infected tigers are likely to present, but other samples 42 detailed understanding of maintenance host identity. Po- 43 that may facilitate diagnosis include lymph node, lung, 43 tential strategies include measures to reduce the density 44 spleen, bladder, urine and whole blood (or fractionated 44 of maintenance populations, or to increase their immune 45 blood containing leucocytes such as buffy coat). Confr- 45 status. Vaccination has been very effective in controlling 46 mation of ante mortem cases can be more challenging, 46 CDV among domestic dogs in many developed coun- 47 as virus may no longer be detectable in the respiratory 47 tries, but may be less successful where a large propor- 48 tract or circulatory system by the time animals present. 48 tion of the dog population is free-roaming and cannot be 49 In such cases detection of virus in conjunctival or respi- 49 restrained (Belsare 2013). Strategies that target unvac- 50 ratory swabs, whole blood or urine would be diagnostic, 50 51 cinated puppies might be more successful, as older dogs 51

1 but negative results need not imply an absence of CDV ACKNOWLEDGMENTS 1 2 infection. 2 We would like to thank the Morris Animal Founda- 3 2. Collect baseline data on the health of wild tigers: Ev- 3 4 tion, Zoo Boise, and the Biotechnology and Biologi- 4 ery effort should be made to take full advantage of op- 5 cal Sciences Research Council for their generous sup- 5 portunities to collect samples from live or dead tigers. 6 port of the project. In addition, none of this work would 6 7 Collection of at least minimal sample sets including se- have been possible without the continued partnership 7 8 rum should take place whenever tigers are handled of the Sikhote-Alin Biosphere Zapovednik (Director D. 8 9 (whether healthy or sick), and post mortem examina- Yu. Gorskhov), Lazovskii Zapovednik (Director A. A. 9 10 tions should be performed (including collection of brain Laptev) and the Russian Ministry of Natural Resources. 10 11 tissue) whenever carcasses are found. Samples need not Thanks also to V. Keahey (In-Sync Exotics) for insights 11 12 be analyzed immediately, particularly where laborato- into the epidemiology of CDV. 12 13 ry resources are limited, but should be archived in se- 13 14 cure facilities and be clearly labeled, sufficient to link REFERENCES 14 15 15 material to corresponding sampling data. Appropriate Alexander KA, McNutt JW, Briggs MB et al. (2010). 16 16 storage includes freezing at or below −20 °C (for se- Multi-host pathogens and carnivore management in 17 17 rum, fresh tissue and samples stored in media for main- southern Africa. Comparative Immunology, Microbi- 18 18 taining nucleic acid such as RNA later) or maintaining ology and Infectious Diseases 33, 249–65. 19 19 at room temperature (for tissues fxed in 10% formalin). 20 Appel MJ, Sheffy B, Percy D, Gaskin J (1974). Canine 20 It should be emphasized that these are minimal sample 21 distemper virus in domestic cats and pigs. American 21 22 sets that would be suffcient to detect antibodies to CDV Journal of Veterinary Research 35, 803–6. 22 23 (indicating prior exposure) or diagnose active CDV in- Appel MJ (1987). Canine Distemper Virus. In: Appel 23 24 fections. More comprehensive sets of diagnostic sam- MJ, ed. Virus Infections of Carnivores. Elsevier Sci- 24 25 ples would enable a more extensive assessment of tiger ence Publishers, Amsterdam, the Netherlands, pp. 25 26 health. However, it is recognized that those involved in 133–59. 26 27 the handling of live or dead tigers often face a variety of Appel MJ, Reggiardo C, Summers BA et al. (1991). Ca- 27 28 constraints, including access to supplies and cold stor- nine distemper virus infection and encephalitis in ja- 28 29 age facilities, expertise and available time. Therefore, velinas (collared peccaries). Archives of Virology 119, 29 30 we encourage wildlife managers to adapt protocols, and 147–52. 30 31 ensure adequate supplies are available to take full ad- Appel MJ, Yates R, Foley G et al. (1994). Canine dis- 31 32 vantage of sampling opportunities in their circumstanc- temper epizootic in lions, tigers, and leopards in 32 33 33 es. North America. Journal of Veterinary Diagnostic In- 34 vestigation 6, 277–88. 34 In the event that CDV is detected in tigers in other ar- 35 Bartlett MS (1960). The Critical Community Size for 35 eas, further research would be required to assess the risk 36 Measles in the United States. Journal of the Royal 36 that this represents at a population level. This could in- 37 Statistical Society: Series A (General) 123, 37–44. 37 38 clude epidemiological modeling, and research direct- 38 Belsare AV (2013). Diseases of free-ranging dogs: Im- 39 ed at the reservoir to determine species composition 39 plications for wildlife conservation in India. Current 40 and dynamics of CDV circulation. Such research would 40 Conservation 7. [Cited 5 Jun 2014.] Available from 41 41 be vital to assessing the need for any intervention, and URL: http://www.currentconservation.org/?q=is- 42 42 to identify control strategies that might be appropriate. sue/7.4. 43 However, ultimately, due to the problems inherent in the 43 44 Belsare AV, Gompper ME (2013). Assessing demo- 44 available control methods, and the limitations of the vi- graphic and epidemiologic parameters of rural dog 45 rus itself to spread, the most viable management strat- 45 46 populations in India during mass vaccination cam- 46 egy would be to maintain tigers in large and inter-con- 47 paigns. Preventive Veterinary Medicine 111, 139–46. 47 nected populations that are able to withstand CDV 48 Biek R, Zarnke RL, Gillin C, Wild M, Squires JR, Poss 48 49 outbreaks should they occur. This recommendation, of M (2002). Serologic survey for viral and bacterial in- 49 50 course, is in concordance with existing conservation fections in western populations of Canada lynx (Lynx 50 51 strategies for most wildlife populations. canadensis). Journal of Wildlife Diseases 38, 840–5. 51

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